Search for Face Identity or Expression: Set Size Effects in Developmental Prosopagnosia.

The set size effect during visual search indexes the effects of processing load and thus the efficiency of perceptual mechanisms. Our goal was to investigate whether individuals with developmental prosopagnosia show increased set size effects when searching faces for face identity and how this compares to search for face expression. We tested 29 healthy individuals and 13 individuals with developmental prosopagnosia. Participants were shown sets of three to seven faces to judge whether the identities or expressions of the faces were the same across all stimuli or if one differed. The set size effect was the slope of the linear regression between the number of faces in the array and the response time. Accuracy was similar in both controls and prosopagnosic participants. Developmental prosopagnosic participants displayed increased set size effects in face identity search but not in expression search. Single-participant analyses reveal that 11 developmental prosopagnosic participants showed a putative classical dissociation, with impairments in identity but not expression search. Signal detection theory analysis showed that identity set size effects were highly reliable in discriminating prosopagnosic participants from controls. Finally, the set size ratios of same to different trials were consistent with the predictions of self-terminated serial search models for control participants and prosopagnosic participants engaged in expression search but deviated from those predictions for identity search by the prosopagnosic cohort. We conclude that the face set size effect reveals a highly prevalent and selective perceptual inefficiency for processing face identity in developmental prosopagnosia.

Looking beyond the face area: lesion network mapping of prosopagnosia.

Damage to the right fusiform face area can disrupt the ability to recognize faces, a classic example of how damage to a specialized brain region can disrupt a specialized brain function. However, similar symptoms can arise from damage to other brain regions, and face recognition is now thought to depend on a distributed brain network. The extent of this network and which regions are critical for facial recognition remains unclear. Here, we derive this network empirically based on lesion locations causing clinically significant impairments in facial recognition. Cases of acquired prosopagnosia were identified through a systematic literature search and lesion locations were mapped to a common brain atlas. The network of brain regions connected to each lesion location was identified using resting state functional connectivity from healthy participants (n = 1000), a technique termed lesion network mapping. Lesion networks were overlapped to identify connections common to lesions causing prosopagnosia. Reproducibility was assessed using split-half replication. Specificity was assessed through comparison with non-specific control lesions (n = 135) and with control lesions associated with symptoms other than prosopagnosia (n = 155). Finally, we tested whether our facial recognition network derived from clinically evident cases of prosopagnosia could predict subclinical facial agnosia in an independent lesion cohort (n = 31). Our systematic literature search identified 44 lesions causing prosopagnosia, only 29 of which intersected the right fusiform face area. However, all 44 lesion locations fell within a single brain network defined by connectivity to the right fusiform face area. Less consistent connectivity was found to other face-selective regions. Surprisingly, all 44 lesion locations were also functionally connected, through negative correlation, with regions in the left frontal cortex. This connectivity pattern was highly reproducible and specific to lesions causing prosopagnosia. Positive connectivity to the right fusiform face area and negative connectivity to left frontal regions were independent predictors of prosopagnosia and predicted subclinical facial agnosia in an independent lesion cohort. We conclude that lesions causing prosopagnosia localize to a single functionally connected brain network defined by connectivity to the right fusiform face area and to left frontal regions. Implications of these findings for models of facial recognition deficits are discussed.

Object recognition in acquired and developmental prosopagnosia.

Whether face and object recognition are dissociated in prosopagnosia continues to be debated: a recent review highlighted deficiencies in prior studies regarding the evidence for such a dissociation. Our goal was to study cohorts with acquired and developmental prosopagnosia with a complementary battery of tests of object recognition that address prior limitations, as well as evaluating for residual effects of object expertise. We studied 15 subjects with acquired and 12 subjects with developmental prosopagnosia on three tests: the Old/New Tests, the Cambridge Bicycle Memory Test, and the Expertise-adjusted Test of Car Recognition. Most subjects with developmental prosopagnosia were normal on the Old/New Tests: for acquired prosopagnosia, subjects with occipitotemporal lesions often showed impairments while those with anterior temporal lesions did not. Ten subjects showed a putative classical dissociation between the Cambridge Face and Bicycle Memory Tests, seven of whom had normal reaction times. Both developmental and acquired groups showed reduced car recognition on the expertise-adjusted test, though residual effects of expertise were still evident. Two subjects with developmental prosopagnosia met criteria for normal object recognition across all tests. We conclude that strong evidence for intact object recognition can be found in a few subjects but the majority show deficits, particularly those with the acquired form. Both acquired and developmental forms show residual but reduced object expertise effects.

The effects of enhanced attention and working memory on smooth pursuit eye movement.

It has long been suggested that increasing attentional demands can alter smooth pursuit eye movements, but the precise nature of the changes generated is not clear. Our goal was to examine smooth pursuit with a task that enhanced attention to the target and that increased demands on working memory, without distracting from the target. 15 subjects tracked a target moving around a predictable circular trajectory at a constant tangential velocity. An n-back task with two levels of additional working memory load was integrated into the pursuit target to increase cognitive demands. In the single-task conditions, subjects either performed pursuit alone or the n-back task with a stationary target. In the dual-task conditions, pursuit and the n-back task were performed together. Performance of the n-back tasks was not impaired by simultaneous smooth pursuit. The n-back tasks had negligible effects on horizontal or vertical pursuit gain, but generated increased phase lag and reduced the variability of position error during pursuit. Increasing the difficulty of the n-back task further reduced the variability of position errors. We conclude that enhanced attention does not alter the velocity gain of smooth pursuit but rather improves its consistency. As long as attention remains focused on the target, increased attentional demands further reduce pursuit variability. Increases in phase lag may serve to improve attentional processing of the target.

Diagnosing Prosopagnosia: The Utility of Visual Noise in the Cambridge Face Recognition Test.

Adding visual noise to facial images has been used to increase reliance on configural processing. Whether this enhances the ability of tests to diagnose prosopagnosia is not known. We examined 15 subjects with developmental prosopagnosia, 13 subjects with acquired prosopagnosia, and 38 control subjects with the Cambridge Face Memory Test. We compared their performance on the second phase, without visual noise, and on the third phase, which adds visual noise. We analyzed the results with signal detection theory methods. The performance of controls worsened more than did that of prosopagnosic subjects when noise was added. The second phase showed better ability to discriminate between prosopagnosic and control subjects than did the third phase. For developmental prosopagnosia, a test using only the 48 trials of the first and second phases yielded sensitivity of 88% and specificity of 91% with a criterion of 33/48 correct, performance characteristics that are similar for a criterion of 43/72 for the whole test. We conclude that a shortened Cambridge Face Memory Test without the noisy images may be a quicker yet equally effective instrument for diagnosing prosopagnosia. The theoretical advantage of noisy images is outweighed by the poorer performance of control subjects with visual noise.

Perceptual Learning of Faces: A Rehabilitative Study of Acquired Prosopagnosia.

Despite many studies of acquired prosopagnosia, there have been only a few attempts at its rehabilitation, all in single cases, with a variety of mnemonic or perceptual approaches, and of variable efficacy. In a cohort with acquired prosopagnosia, we evaluated a perceptual learning program that incorporated variations in view and expression, which was aimed at training perceptual stages of face processing with an emphasis on ecological validity. Ten patients undertook an 11-week face training program and an 11-week control task. Training required shape discrimination between morphed facial images, whose similarity was manipulated by a staircase procedure to keep training near a perceptual threshold. Training progressed from blocks of neutral faces in frontal view through increasing variations in view and expression. Whereas the control task did not change perception, training improved perceptual sensitivity for the trained faces and generalized to new untrained expressions and views of those faces. There was also a significant transfer to new faces. Benefits were maintained over a 3-month period. Training efficacy was greater for those with more perceptual deficits at baseline. We conclude that perceptual learning can lead to persistent improvements in face discrimination in acquired prosopagnosia. This reflects both acquisition of new skills that can be applied to new faces as well as a degree of overlearning of the stimulus set at the level of 3-D expression-invariant representations.

Word and text processing in developmental prosopagnosia.

The "many-to-many" hypothesis proposes that visual object processing is supported by distributed circuits that overlap for different object categories. For faces and words the hypothesis posits that both posterior fusiform regions contribute to both face and visual word perception and predicts that unilateral lesions impairing one will affect the other. However, studies testing this hypothesis have produced mixed results. We evaluated visual word processing in subjects with developmental prosopagnosia, a condition linked to right posterior fusiform abnormalities. Ten developmental prosopagnosic subjects performed a word-length effect task and a task evaluating the recognition of word content across variations in text style, and the recognition of style across variations in word content. All subjects had normal word-length effects. One had prolonged sorting time for word recognition in handwritten stimuli. These results suggest that the deficit in developmental prosopagnosia is unlikely to affect visual word processing, contrary to predictions of the many-to-many hypothesis.

Measuring young infants' sensitivity to height-in-the-picture-plane by contrasting monocular and binocular preferential-looking.

To examine young infants' sensitivity to a pictorial depth cue, we compared monocular and binocular preferential looking to objects of which depth was specified by height-in-the-picture-plane. For adults, this cue generates the perception that a lower object is closer than a higher object. This study showed that 4- and 5-month-old infants fixated the lower, apparently closer, figure more often under the monocular than binocular presentation providing evidence of their sensitivity to the pictorial depth cue. Because the displays were identical in the two conditions except for binocular information for depth, the difference in looking-behavior indicated sensitivity to depth information, excluding a possibility that they responded to 2D characteristics. This study also confirmed the usefulness of the method, preferential looking with a monocular and binocular comparison, to examine sensitivity to a pictorial depth cue in young infants, who are too immature to reach reliably for the closer of two objects.

Effects of Voice and Biographic Data on Face Encoding.

There are various perceptual and informational cues for recognizing people. How these interact in the recognition process is of interest. Our goal was to determine if the encoding of faces was enhanced by the concurrent presence of a voice, biographic data, or both. Using a between-subject design, four groups of 10 subjects learned the identities of 24 faces seen in video-clips. Half of the faces were seen only with their names, while the other half had additional information. For the first group this was the person's voice, for the second, it was biographic data, and for the third, both voice and biographic data. In a fourth control group, the additional information was the voice of a generic narrator relating non-biographic information. In the retrieval phase, subjects performed a familiarity task and then a face-to-name identification task with dynamic faces alone. Our results consistently showed no benefit to face encoding with additional information, for either the familiarity or identification task. Tests for equivalency indicated that facilitative effects of a voice or biographic data on face encoding were not likely to exceed 3% in accuracy. We conclude that face encoding is minimally influenced by cross-modal information from voices or biographic data.

Music perception in acquired prosopagnosia.

BACKGROUND: Acquired prosopagnosia is often associated with other deficits such as dyschromatopsia and topographagnosia, from damage to adjacent perceptual networks. A recent study showed that some subjects with developmental prosopagnosia also have congenital amusia, but problems with music perception have not been described with the acquired variant. OBJECTIVE: Our goal was to determine if music perception was also impaired in subjects with acquired prosopagnosia, and if so, its anatomic correlate. METHOD: We studied eight subjects with acquired prosopagnosia, all of whom had extensive neuropsychological and neuroimaging testing. They performed a battery of tests evaluating pitch and rhythm processing, including the Montréal Battery for the Evaluation of Amusia. RESULTS: At the group level, subjects with anterior temporal lesions were impaired in pitch perception relative to the control group, but not those with occipitotemporal lesions. Three of eight subjects with acquired prosopagnosia had impaired musical pitch perception while rhythm perception was spared. Two of the three also showed reduced musical memory. These three reported alterations in their emotional experience of music: one reported music anhedonia and aversion, while the remaining two had changes consistent with musicophilia. The lesions of these three subjects affected the right or bilateral temporal poles as well as the right amygdala and insula. None of the three prosopagnosic subjects with lesions limited to the inferior occipitotemporal cortex exhibited impaired pitch perception or musical memory, or reported changes in music appreciation. CONCLUSION: Together with the results of our previous studies of voice recognition, these findings indicate an anterior ventral syndrome that can include the amnestic variant of prosopagnosia, phonagnosia, and various alterations in music perception, including acquired amusia, reduced musical memory, and subjective reports of altered emotional experience of music.

The role of the upper and lower face in the recognition of facial identity in dynamic stimuli.

Studies with static faces find that upper face halves are more easily recognized than lower face halves-an upper-face advantage. However, faces are usually encountered as dynamic stimuli, and there is evidence that dynamic information influences face identity recognition. This raises the question of whether dynamic faces also show an upper-face advantage. The objective of this study was to examine whether familiarity for recently learned faces was more accurate for upper or lower face halves, and whether this depended upon whether the face was presented as static or dynamic. In Experiment 1, subjects learned a total of 12 faces--6 static images and 6 dynamic video-clips of actors in silent conversation. In experiment 2, subjects learned 12 faces, all dynamic video-clips. During the testing phase of Experiments 1 (between subjects) and 2 (within subjects), subjects were asked to recognize upper and lower face halves from either static images and/or dynamic clips. The data did not provide evidence for a difference in the upper-face advantage between static and dynamic faces. However, in both experiments, we found an upper-face advantage, consistent with prior literature, for female faces, but not for male faces. In conclusion, the use of dynamic stimuli may have little effect on the presence of an upper-face advantage, especially when the static comparison contains a series of static images, rather than a single static image, and is of sufficient image quality. Future studies could investigate the influence of face gender on the presence of an upper-face advantage.

Developmental prosopagnosia in childhood.

Developmental prosopagnosia (DP) is defined by severe face recognition problems resulting from a failure to develop the necessary visual mechanisms for processing faces. While there is a growing literature on DP in adults, little has been done to study this disorder in children. The profound impact of abnormal face perception on social functioning and the general lack of awareness of childhood DP can result in severe social and psychological consequences for children. This review discusses possible aetiologies of DP and summarizes the few cases of childhood DP that have been reported. It also outlines key objectives for the growth of this emerging research area and special considerations for studying DP in children. With clear goals and concerted efforts, the study of DP in childhood will be an exciting avenue for enhancing our understanding of normal and abnormal face perception for all age groups.

Infants and adults use line junction information to perceive 3D shape.

Two experiments investigated infants' and adults' perception of 3D shape from line junction information. Participants in both experiments viewed a concave wire half-cube frame. In Experiment 1, adults reported that the concave wire frame appeared to be convex when it was viewed monocularly (with one eye covered) and that it appeared to be concave when it was viewed binocularly. In Experiment 2, 5- and 7-month-old infants were shown the concave wire frame under monocular and binocular viewing conditions, and their reaching behavior was recorded. The infants in both age groups reached preferentially toward the center of the wire frame in the monocular condition and toward its edges in the binocular condition. Because infants typically reach to what they perceive to be closest to them, these reaching preferences provide evidence that they perceived the wire frame as convex when they viewed it monocularly and as concave when they viewed it binocularly. These findings suggest that, by 5 months of age, infants, like adults, use line junction information to perceive depth and object shape.

Facial identity and facial speech processing in developmental prosopagnosia.

The neural substrate of acquired prosopagnosia, including its lateralization, remains a matter of investigation. Face processing networks in healthy subjects are right dominant, and acquired prosopagnosia usually results from right or bilateral lesions. Nevertheless, there may be a complementary contribution of the left hemisphere to certain types of face processing. Prior reports suggest that this might be processing faces depicted by line contours, or lip reading. We performed two behavioural studies in seven subjects with developmental prosopagnosia. The first examined their ability to match faces across viewpoint changes, with either unaltered photographs or images that had been reduced to line elements. Prosopagnosic subjects had normal performance with line-contour faces, but failed to show the normal benefit from the additional information in unaltered photographs. The second experiment examined their ability to perceive facial speech patterns. Prosopagnosic subjects could detect, discriminate and identify facial speech patterns, but most showed reduced use of these cues or anomalous audiovisual integration in the McGurk effect, with only one subject performing normally. We conclude that developmental prosopagnosia can be associated with a subtle impairment in lip reading, which in prior studies of acquired lesions has been associated more with left than with right fusiform damage.

Effects of Faces and Voices on the Encoding of Biographic Information.

There are multiple forms of knowledge about people. Whether diverse person-related data interact is of interest regarding the more general issue of integration of multi-source information about the world. Our goal was to examine whether perception of a person's face or voice enhanced the encoding of their biographic data. We performed three experiments. In the first experiment, subjects learned the biographic data of a character with or without a video clip of their face. In the second experiment, they learned the character's data with an audio clip of either a generic narrator's voice or the character's voice relating the same biographic information. In the third experiment, an audiovisual clip of both the face and voice of either a generic narrator or the character accompanied the learning of biographic data. After learning, a test phase presented biographic data alone, and subjects were tested first for familiarity and second for matching of biographic data to the name. The results showed equivalent learning of biographic data across all three experiments, and none showed evidence that a character's face or voice enhanced the learning of biographic information. We conclude that the simultaneous processing of perceptual representations of people may not modulate the encoding of biographic data.

Prosopagnosia and disorders of face processing.

Face recognition is a form of expert visual processing. Acquired prosopagnosia is the loss of familiarity for facial identity and has several functional variants, namely apperceptive, amnestic, and associative forms. Acquired forms are usually caused by either occipitotemporal or anterior temporal lesions, right or bilateral in most cases. In addition, there is a developmental form, whose functional and structural origins are still being elucidated. Despite their difficulties with recognizing faces, some of these subjects still show signs of covert recognition, which may have a number of explanations. Other aspects of face perception can be spared in prosopagnosic subjects. Patients with other types of face processing difficulties have been described, including impaired expression processing, impaired lip-reading, false familiarity for faces, and a people-specific amnesia. Recent rehabilitative studies have shown some modest ability to improve face perception in prosopagnosic subjects through perceptual training protocols.

The development of the ability of infants to utilize static cues to create and access representations of object shape.

A "transfer-across-depth-cues" method was used to explore the development of the ability to generate and use spatial representations of an object as specified by static pictorial depth cues. Infants were habituated to an object with depth specified by one cue and then presented with the same shape with depth specified by a different cue. Only if an abstract representation of that object had been formed could transfer across cues occur. Shading and line junctions uniquely determined the 3D shapes in these displays so that they appeared to be either a slice of cake with a flat top or a rocket. Without these cues, both line drawings were identical. Infants aged 6 to 7 months showed significant evidence of transfer, while infants aged 4 to 5 months did not. A control experiment demonstrated that the younger infants could discriminate between the objects when a single depth cue specified the shapes. These results are similar to our previous findings, which indicated that 6- to 7-month-old infants show transfer across shading and surface-contour cues, specifying convex and concave surfaces (A. Tsuruhara, T. Sawada, S. Kanazawa, M. K. Yamaguchi, & A. Yonas, 2009). This work supports the hypothesis that the ability to form 3D spatial representations from pictorial depth cues develops at about 6 months of age.

The Scanpaths of Subjects with Developmental Prosopagnosia during a Face Memory Task.

The scanpaths of healthy subjects show biases towards the upper face, the eyes and the center of the face, which suggests that their fixations are guided by a feature hierarchy towards the regions most informative for face identification. However, subjects with developmental prosopagnosia have a lifelong impairment in face processing. Whether this is reflected in the loss of normal face-scanning strategies is not known. The goal of this study was to determine if subjects with developmental prosopagnosia showed anomalous scanning biases as they processed the identity of faces. We recorded the fixations of 10 subjects with developmental prosopagnosia as they performed a face memorization and recognition task, for comparison with 8 subjects with acquired prosopagnosia (four with anterior temporal lesions and four with occipitotemporal lesions) and 20 control subjects. The scanning of healthy subjects confirmed a bias to fixate the upper over the lower face, the eyes over the mouth, and the central over the peripheral face. Subjects with acquired prosopagnosia from occipitotemporal lesions had more dispersed fixations and a trend to fixate less informative facial regions. Subjects with developmental prosopagnosia did not differ from the controls. At a single-subject level, some developmental subjects performed abnormally, but none consistently across all metrics. Scanning distributions were not related to scores on perceptual or memory tests for faces. We conclude that despite lifelong difficulty with faces, subjects with developmental prosopagnosia still have an internal facial schema that guides their scanning behavior.

Training face perception in developmental prosopagnosia through perceptual learning.

BACKGROUND: Recent work has shown that perceptual learning can improve face discrimination in subjects with acquired prosopagnosia. OBJECTIVE: In this study, we administered the same program to determine if such training would improve face perception in developmental prosopagnosia. METHOD: We trained ten subjects with developmental prosopagnosia for several months with a program that required shape discrimination between morphed facial images, using a staircase procedure to keep training near each subject's perceptual threshold. To promote ecological validity, training progressed from blocks of neutral faces in frontal view through increasing variations in view and expression. Five subjects did 11 weeks of a control television task before training, and the other five were re-assessed for maintenance of benefit 3 months after training. RESULTS: Perceptual sensitivity for faces improved after training but did not improve after the control task. Improvement generalized to untrained expressions and views of these faces, and there was some evidence of transfer to new faces. Benefits were maintained over three months. Training also led to improvements on standard neuropsychological tests of short-term familiarity, and some subjects reported positive effects in daily life. CONCLUSION: We conclude that perceptual learning can lead to persistent improvements in face discrimination in developmental prosopagnosia. The strong generalization suggests that learning is occurring at the level of three-dimensional representations with some invariance for the dynamic effects of expression.

Perception of musical pitch in developmental prosopagnosia.

Studies of developmental prosopagnosia have often shown that developmental prosopagnosia differentially affects human face processing over non-face object processing. However, little consideration has been given to whether this condition is associated with perceptual or sensorimotor impairments in other modalities. Comorbidities have played a role in theories of other developmental disorders such as dyslexia, but studies of developmental prosopagnosia have often focused on the nature of the visual recognition impairment despite evidence for widespread neural anomalies that might affect other sensorimotor systems. We studied 12 subjects with developmental prosopagnosia with a battery of auditory tests evaluating pitch and rhythm processing as well as voice perception and recognition. Overall, three subjects were impaired in fine pitch discrimination, a prevalence of 25% that is higher than the estimated 4% prevalence of congenital amusia in the general population. This was a selective deficit, as rhythm perception was unaffected in all 12 subjects. Furthermore, two of the three prosopagnosic subjects who were impaired in pitch discrimination had intact voice perception and recognition, while two of the remaining nine subjects had impaired voice recognition but intact pitch perception. These results indicate that, in some subjects with developmental prosopagnosia, the face recognition deficit is not an isolated impairment but is associated with deficits in other domains, such as auditory perception. These deficits may form part of a broader syndrome which could be due to distributed microstructural anomalies in various brain networks, possibly with a common theme of right hemispheric predominance.