Voice Recognition in Face-Blind Patients.

Right or bilateral anterior temporal damage can impair face recognition, but whether this is an associative variant of prosopagnosia or part of a multimodal disorder of person recognition is an unsettled question, with implications for cognitive and neuroanatomic models of person recognition. We assessed voice perception and short-term recognition of recently heard voices in 10 subjects with impaired face recognition acquired after cerebral lesions. All 4 subjects with apperceptive prosopagnosia due to lesions limited to fusiform cortex had intact voice discrimination and recognition. One subject with bilateral fusiform and anterior temporal lesions had a combined apperceptive prosopagnosia and apperceptive phonagnosia, the first such described case. Deficits indicating a multimodal syndrome of person recognition were found only in 2 subjects with bilateral anterior temporal lesions. All 3 subjects with right anterior temporal lesions had normal voice perception and recognition, 2 of whom performed normally on perceptual discrimination of faces. This confirms that such lesions can cause a modality-specific associative prosopagnosia.

Developmental phonagnosia: Neural correlates and a behavioral marker.

A 20-year old female, AN, with no history of neurological events or detectable lesions, was markedly poorer than controls at identifying her most familiar celebrity voices. She was normal at face recognition and in discriminating which of two speakers uttered a particular sentence. She evidences normal fMRI sensitivity for human speech and non-speech sounds. AN, and two other phonagnosics, were unable to imagine the voices of highly familiar individuals. A region in the ventromedial prefrontal cortex (vmPFC) was differentially activated in controls when imagining familiar celebrity voices compared to imagining non-voice sounds. AN evidenced no differential activation in this area, which has been termed a person identity semantic system. Rather than a deficit in the representation of voice-individuating cues, AN may be unable to associate those cues to the identity of a familiar person. In this respect, the deficit in developmental phonagnosia may bear a striking parallel to developmental prosopagnosia.

Holistic face training enhances face processing in developmental prosopagnosia.

Prosopagnosia has largely been regarded as an untreatable disorder. However, recent case studies using cognitive training have shown that it is possible to enhance face recognition abilities in individuals with developmental prosopagnosia. Our goal was to determine if this approach could be effective in a larger population of developmental prosopagnosics. We trained 24 developmental prosopagnosics using a 3-week online face-training program targeting holistic face processing. Twelve subjects with developmental prosopagnosia were assessed before and after training, and the other 12 were assessed before and after a waiting period, they then performed the training, and were then assessed again. The assessments included measures of front-view face discrimination, face discrimination with view-point changes, measures of holistic face processing, and a 5-day diary to quantify potential real-world improvements. Compared with the waiting period, developmental prosopagnosics showed moderate but significant overall training-related improvements on measures of front-view face discrimination. Those who reached the more difficult levels of training ('better' trainees) showed the strongest improvements in front-view face discrimination and showed significantly increased holistic face processing to the point of being similar to that of unimpaired control subjects. Despite challenges in characterizing developmental prosopagnosics' everyday face recognition and potential biases in self-report, results also showed modest but consistent self-reported diary improvements. In summary, we demonstrate that by using cognitive training that targets holistic processing, it is possible to enhance face perception across a group of developmental prosopagnosics and further suggest that those who improved the most on the training task received the greatest benefits.

Functional connectivity between face-movement and speech-intelligibility areas during auditory-only speech perception.

It has been proposed that internal simulation of the talking face of visually-known speakers facilitates auditory speech recognition. One prediction of this view is that brain areas involved in auditory-only speech comprehension interact with visual face-movement sensitive areas, even under auditory-only listening conditions. Here, we test this hypothesis using connectivity analyses of functional magnetic resonance imaging (fMRI) data. Participants (17 normal participants, 17 developmental prosopagnosics) first learned six speakers via brief voice-face or voice-occupation training (<2 min/speaker). This was followed by an auditory-only speech recognition task and a control task (voice recognition) involving the learned speakers' voices in the MRI scanner. As hypothesized, we found that, during speech recognition, familiarity with the speaker's face increased the functional connectivity between the face-movement sensitive posterior superior temporal sulcus (STS) and an anterior STS region that supports auditory speech intelligibility. There was no difference between normal participants and prosopagnosics. This was expected because previous findings have shown that both groups use the face-movement sensitive STS to optimize auditory-only speech comprehension. Overall, the present findings indicate that learned visual information is integrated into the analysis of auditory-only speech and that this integration results from the interaction of task-relevant face-movement and auditory speech-sensitive areas.

Visual body recognition in a prosopagnosic patient.

Conspicuous deficits in face recognition characterize prosopagnosia. Information on whether agnosic deficits may extend to non-facial body parts is lacking. Here we report the neuropsychological description of FM, a patient affected by a complete deficit in face recognition in the presence of mild clinical signs of visual object agnosia. His deficit involves both overt and covert recognition of faces (i.e. recognition of familiar faces, but also categorization of faces for gender or age) as well as the visual mental imagery of faces. By means of a series of matching-to-sample tasks we investigated: (i) a possible association between prosopagnosia and disorders in visual body perception; (ii) the effect of the emotional content of stimuli on the visual discrimination of faces, bodies and objects; (iii) the existence of a dissociation between identity recognition and the emotional discrimination of faces and bodies. Our results document, for the first time, the co-occurrence of body agnosia, i.e. the visual inability to discriminate body forms and body actions, and prosopagnosia. Moreover, the results show better performance in the discrimination of emotional face and body expressions with respect to body identity and neutral actions. Since FM's lesions involve bilateral fusiform areas, it is unlikely that the amygdala-temporal projections explain the relative sparing of emotion discrimination performance. Indeed, the emotional content of the stimuli did not improve the discrimination of their identity. The results hint at the existence of two segregated brain networks involved in identity and emotional discrimination that are at least partially shared by face and body processing.

Holistic processing of the mouth but not the eyes in developmental prosopagnosia.

Because holistic processing is a hallmark of normal face recognition, we ask whether such processing is reduced in developmental prosopagnosia (DP), and, if so, what the sources are of this deficit. Existing literature provides a mixed picture, with face inversion effects showing consistent holistic processing deficits but unable to locate their source and with some composite face studies showing reduced holistic processing and some not. We addressed this issue more thoroughly with a very large sample of DPs (N = 38) performing the part-whole task, a well-accepted measure of holistic processing that allows for the separate evaluation of individual face parts. Contrary to an expected overall reduction in holistic processing, we found an intact holistic advantage for the mouth and a complete absence of a holistic advantage for the eye region. Less severely impaired prosopagnosics showed significantly more holistic processing of the mouth, suggesting that holistic processing can aid them in recognizing faces.

Perceptual separability of featural and configural information in congenital prosopagnosia.

The deficit in face recognition in individuals with prosopagnosia has often been attributed to an underlying impairment in holistic processing. Exactly what constitutes holistic processing has remained controversial, however. Here, we compare how configural information and featural information interact during face processing in a group of individuals with congenital prosopagnosia (CP) and matched controls. We adopted Amishav and Kimchi's version of Garner's speeded classification task, in which observers classify upright faces based on configural (intereyes and nose-mouth spacing) or featural (shape of eyes, nose, and mouth) information while the other dimension remains constant or varied randomly. We replicated the finding that normal observers evince symmetric Garner interference--failure to selectively attend to features without being influenced by irrelevant variation in configuration, and vice versa--indicating that featural and configural information are integral in normal face processing. In contrast, the CPs showed no Garner interference: They were able to attend to configural information without interference from irrelevant variation in featural information, and they were able to attend to featural information without interference from irrelevant variation in configural information. The absence of Garner interference in CP provides strong evidence that featural information and configural information are perceptually separable in CP's face processing. These findings indicate that CPs do not perceive faces holistically; rather, they process featural and configural information independently.

Impaired holistic processing in congenital prosopagnosia.

It has long been argued that face processing requires disproportionate reliance on holistic or configural processing, relative to that required for non-face object recognition, and that a disruption of such holistic processing may be causally implicated in prosopagnosia. Previously, we demonstrated that individuals with congenital prosopagnosia (CP) did not show the normal face inversion effect (better performance for upright compared to inverted faces) and evinced a local (rather than the normal global) bias in a compound letter global/local (GL) task, supporting the claim of disrupted holistic processing in prosopagnosia. Here, we investigate further the nature of holistic processing impairments in CP, first by confirming, in a large sample of CP individuals, the absence of the normal face inversion effect and the presence of the local bias on the GL task, and, second, by employing the composite face paradigm, often regarded as the gold standard for measuring holistic face processing. In this last task, we show that, in contrast with controls, the CP group perform equivalently with aligned and misaligned faces and was impervious to (the normal) interference from the task-irrelevant bottom part of faces. Interestingly, the extent of the local bias evident in the composite task is correlated with the abnormality of performance on diagnostic face processing tasks. Furthermore, there is a significant correlation between the magnitude of the local bias in the GL and performance on the composite task. These results provide further evidence for impaired holistic processing in CP and, moreover, corroborate the critical role of this type of processing for intact face recognition.

Training with own-race faces can improve processing of other-race faces: evidence from developmental prosopagnosia.

Faces of one's own race are discriminated and recognized more accurately than faces of an other race (other-race effect - ORE). Studies have employed several methods to enhance individuation and recognition of other-race faces and reduce the ORE, including intensive perceptual training with other-race faces and explicitly instructing participants to individuate other-race faces. Unfortunately, intensive perceptual training has shown to be specific to the race trained and the use of explicit individuation strategies, though applicable to all races, can be demanding of attention and difficult to consistently employ. It has not yet been demonstrated that a training procedure can foster the automatic individuation of all other-race faces, not just faces from the race trained. Anecdotal evidence from a training procedure used with developmental prosopagnosics (DPs) in our lab, individuals with lifelong face recognition impairments, suggests that this may be possible. To further test this idea, we had five Caucasian DPs perform ten days of configural face training (i.e. attending to small spacing differences between facial features) with own-race (Caucasian) faces to see if training would generalize to improvements with other-race (Korean) faces. To assess training effects and localize potential effects to parts-based or holistic processing, we used the part-whole task using Caucasian and Korean faces (Tanaka, J. W., Kiefer, M., & Bukach, C. M. (2004). A holistic account of the own-race effect in face recognition: evidence from a cross-cultural study. Cognition, 93(1), B1-9). Results demonstrated that after training, DPs showed a disproportionate improvement in holistic processing of other-race faces compared to own-race faces, reducing their ORE. This suggests that configural training with own-race faces boosted DPs' general configural/holistic attentional resources, which they were able to apply to other-race faces. This provides a novel method to reduce the ORE and supports more of an attentional/social-cognitive model of the ORE rather than a strictly expertise model.

Superior voice recognition in a patient with acquired prosopagnosia and object agnosia.

Anecdotally, it has been reported that individuals with acquired prosopagnosia compensate for their inability to recognize faces by using other person identity cues such as hair, gait or the voice. Are they therefore superior at the use of non-face cues, specifically voices, to person identity? Here, we empirically measure person and object identity recognition in a patient with acquired prosopagnosia and object agnosia. We quantify person identity (face and voice) and object identity (car and horn) recognition for visual, auditory, and bimodal (visual and auditory) stimuli. The patient is unable to recognize faces or cars, consistent with his prosopagnosia and object agnosia, respectively. He is perfectly able to recognize people's voices and car horns and bimodal stimuli. These data show a reverse shift in the typical weighting of visual over auditory information for audiovisual stimuli in a compromised visual recognition system. Moreover, the patient shows selectively superior voice recognition compared to the controls revealing that two different stimulus domains, persons and objects, may not be equally affected by sensory adaptation effects. This also implies that person and object identity recognition are processed in separate pathways. These data demonstrate that an individual with acquired prosopagnosia and object agnosia can compensate for the visual impairment and become quite skilled at using spared aspects of sensory processing. In the case of acquired prosopagnosia it is advantageous to develop a superior use of voices for person identity recognition in everyday life.

A comparative case study of face recognition: the contribution of configural and part-based recognition systems, and their interaction.

Understanding the interaction between the configural and part-based systems in face recognition is the major aim of this study. Specifically, we established whether configural representation of faces contribute to aspects of face recognition that depend on part-based processes, such as identifying inverted or fractured faces. Using face recognition tasks that require part-based or configural processing, we compared the results of CK--a man who has object agnosia and alexia [Moscovitch, M., Winocur, G., & Behrmann, M. (1997). What is special about face recognition? Nineteen experiments on a person with visual object agnosia and dyslexia but normal face recognition. Journal of Cognitive Neuroscience, 9(5), 555-604] but normal upright face recognition, to those of DC--a man who has prosopagnosia but normal object recognition. CK was normal at recognizing faces if configural processing was sufficient, but poor at recognizing faces that were modified so as to alter their gestalt, and require part-based processing (Moscovitch et al.). DC was impaired at recognizing upright faces and his performance declined in all tasks involving recognition of modified faces, including those that depend on part-based and on configural processing. Nevertheless, DC was normal on tasks involving perception of generic faces and face imagery. These results show that although configural face perception can proceed without part-based processing, the reverse is not the case. Our results suggest that the configural system is always necessary for face recognition, and appears to support what remains of face identification even in prosopagnosic people who have an intact part-based system.

Hereditary prosopagnosia: the first case series.

Prosopagnosia is defined as a specific type of visual agnosia characterised by a discernible impairment in the capacity to recognise familiar people by their faces. We present seven family pedigrees with 38 cases in two to four generations of suspected hereditary prosopagnosia, detected using a screening questionnaire. Men and women are impaired and the anomaly is regularly transmitted from generation to generation in all pedigrees studied. Segregation is best explained by a simple autosomal dominant mode of inheritance, suggesting that loss of human face recognition can occur by the mutation of a single gene. Eight of the 38 affected persons were tested on the Warrington Recognition Memory Test for Faces (RMF; Warrington, 1984), famous and family faces tests, learning tests for internal and external facial features and a measure of mental imagery for face and non-face images. As a group, the eight participants scored significantly below an age- and education-matched comparison group on the most relevant test of face recognition; and all were impaired on at least one of the tests. The results provide compelling evidence for significant genetic contribution to face recognition skills and contribute to the promise offered by the emerging field of cognitive neurogenetics.

Scan patterns during the processing of facial identity in prosopagnosia.

The scan patterns of ocular fixations made by prosopagnosic patients while they attempt to identify faces may provide insights into how they process the information in faces. Contrasts between their scanning of upright versus inverted faces may index the presence of a hypothesized orientation-dependent expert mechanism for processing faces, while contrasts between their scanning of familiar versus novel faces may index the influence of residual facial memories on their search for meaningful facial information. We recorded the eye movements of two prosopagnosics while they viewed faces. One patient, with acquired prosopagnosia from a right occipitotemporal lesion, showed degraded orientation effects but still with a normal distribution of fixations to more salient facial features. However, the dynamics of his global scan patterns were more chaotic for novel faces, suggesting degradation of an internal facial schema, and consistent with other evidence of impaired face configuration perception in this patient. His global scan patterns for famous faces differed from novel faces, suggesting the influence of residual facial memories, as indexed previously by his relatively good imagery for famous faces. The other patient, with a developmental prosopagnosia, showed anomalous orientation effects, abnormal distribution of fixations to less salient regions, and chaotic global scan patterns, in keeping with a more severe loss of face-expert mechanisms. The effects of fame on her scanning were weaker than those in the first subject and non-existent in her global scan patterns. We conclude that scan patterns in prosopagnosia can both reflect the loss of orientation-dependent expert mechanisms and index the covert influence of residual facial memories. In these two subjects the scanning data were consistent with other results from tests of configuration perception, imagery, and covert recognition.

Can generic expertise explain special processing for faces?

Does face recognition involve face-specific cognitive and neural processes ('domain specificity') or do faces only seem special because people have had more experience of individuating them than they have of individuating members of other homogeneous object categories ('the expertise hypothesis')? Here, we summarize new data that test these hypotheses by assessing whether classic face-selective effects - holistic processing, recognition impairments in prosopagnosia and fusiform face area activation - remain face selective in comparison with objects of expertise. We argue that evidence strongly supports domain specificity rather than the expertise hypothesis. We conclude that the crucial social function of face recognition does not reflect merely a general practice phenomenon and that it might be supported by evolved mechanisms (visual or nonvisual) and/or a sensitive period in infancy.

Voice recognition and cross-modal responses to familiar speakers' voices in prosopagnosia.

Recognizing the voices of people we know does not only activate "voice areas" in the temporal lobe but also extraauditory areas including the fusiform "face area" (FFA). This cross-modal effect could reflect that individual face and voice information become specifically associated when becoming acquainted with a person. Here, we addressed whether the ability to have individual face representations 1) plays a role in voice recognition and 2) is required to observe cross-modal responses to voices in face areas. We compared speaker recognition performance and neuroimaging responses during the processing of familiar and nonfamiliar speakers' voices in a developmental prosopagnosic subject (SO) with the respective findings obtained in a group of 9 control subjects. Despite scoring worse than controls on recognition of familiar speakers' voices, SO had normal cross-modal responses in the FFA and normal connectivity between FFA and the voice regions. However, she had reduced activations in areas that usually respond to familiarity with people. An indication for the malfunctioning of her FFA was reduced connectivity of the FFA to a subset of these supramodal areas. In combination these data suggest that 1) voice recognition benefits from the ability to process faces at an individual level and 2) cross-modal association of voices and faces in the brain is achieved by a sensory binding and does not depend on a top-down mechanism subsequent to successful person recognition.

Face imagery and its relation to perception and covert recognition in prosopagnosia.

BACKGROUND: Face imagery can access facial memories without the use of perceptual stimuli. Current data on the relation of imagery to the perceptual function and neuroanatomy of prosopagnosic patients are mixed, and little is known about the type of facial information patients can access through imagery. OBJECTIVE: The authors wished to determine 1) which lesions abolished face imagery in prosopagnosia, 2) if deficits in perceiving facial structure were paralleled by similar deficits in imagery, and 3) if covert recognition of faces correlated with the degree of residual imagery for faces. METHODS: The authors tested nine prosopagnosic patients who had been tested previously for perception of facial configuration and covert recognition of famous faces. The authors constructed a battery of 37 questions that asked subjects to imagine the faces of two celebrities and to choose which one had a certain facial property. Half were questions about facial features and half were about overall facial shape. RESULTS: Imagery was abolished only by anterior temporal lesions. Imagery for facial shape but not features was degraded by lesions of the right hemisphere's fusiform face area, which severely impaired perception of facial configuration. Feature imagery was degraded only when there was associated left occipito-temporal damage. Covert recognition was found when either configural perception or imagery was severely damaged, but not when both were abnormal. In patients with impaired configural perception, covert recognition correlated with feature imagery, suggesting that feature-based processing may drive residual covert abilities in these patients. CONCLUSION: Although anterior temporal cortex may be the site of facial memory stores, these data also support hypotheses that perceptual areas like the fusiform face area have parallel contributions to mental imagery. The data on covert recognition are consistent with a view that it is the residue of a partially damaged face-recognition network. Covert recognition may reflect the degree of damage across components of a network rather than mark a specific form of prosopagnosia or a dissociated pathway.

Covert processing of faces in prosopagnosia is restricted to facial expressions: evidence from cross-modal bias.

We present a single case study of a brain-damaged patient, AD, suffering from visual face and object agnosia, with impaired visual perception and preserved mental imagery. She is severely impaired in all aspects of overt recognition of faces as well as in covert recognition of familiar faces. She shows a complete loss of processing facial expressions in recognition as well as in matching tasks. Nevertheless, when presented with a task where face and voice expressions were presented concurrently, there was a clear impact of face expressions on her ratings of the voice. The cross-modal paradigm used here and validated previously with normal subjects (de Gelder & Vroomen, 1995, 2000), appears as a useful tool in investigating spared covert face processing in a neuropsychological perspective, especially with prosopagnosic patients. These findings are discussed against the background of different models of the covert recognition of face expressions.