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Face processing is mediated by interactions between functional areas in the occipital and temporal lobe, and the fusiform face area (FFA) and anterior temporal lobe play key roles in the recognition of facial identity. Individuals with developmental prosopagnosia (DP), a lifelong face recognition impairment, have been shown to have structural and functional neuronal alterations in these areas. The present study investigated how face selectivity is generated in participants with normal face processing, and how functional abnormalities associated with DP, arise as a function of network connectivity. Using functional magnetic resonance imaging and dynamic causal modeling, we examined effective connectivity in normal participants by assessing network models that include early visual cortex (EVC) and face-selective areas and then investigated the integrity of this connectivity in participants with DP. Results showed that a feedforward architecture from EVC to the occipital face area, EVC to FFA, and EVC to posterior superior temporal sulcus (pSTS) best explained how face selectivity arises in both controls and participants with DP. In this architecture, the DP group showed reduced connection strengths on feedforward connections carrying face information from EVC to FFA and EVC to pSTS. These altered network dynamics in DP contribute to the diminished face selectivity in the posterior occipitotemporal areas affected in DP. These findings suggest a novel view on the relevance of feedforward projection from EVC to posterior occipitotemporal face areas in generating cortical face selectivity and differences in face recognition ability. SIGNIFICANCE STATEMENT: Areas of the human brain showing enhanced activation to faces compared to other objects or places have been extensively studied. However, the factors leading to this face selectively have remained mostly unknown. We show that effective connectivity from early visual cortex to posterior occipitotemporal face areas gives rise to face selectivity. Furthermore, people with developmental prosopagnosia, a lifelong face recognition impairment, have reduced face selectivity in the posterior occipitotemporal face areas and left anterior temporal lobe. We show that this reduced face selectivity can be predicted by effective connectivity from early visual cortex to posterior occipitotemporal face areas. This study presents the first network-based account of how face selectivity arises in the human brain.

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While a network of cortical regions contribute to face processing, the lesions in acquired prosopagnosia are highly variable, and likely result in different combinations of spared and affected regions of this network. To assess the residual functional sensitivities of spared regions in prosopagnosia, we designed a rapid event-related functional magnetic resonance imaging (fMRI) experiment that included pairs of faces with same or different identities and same or different expressions. By measuring the release from adaptation to these facial changes we determined the residual sensitivity of face-selective regions-of-interest. We tested three patients with acquired prosopagnosia, and all three of these patients demonstrated residual sensitivity for facial identity changes in surviving fusiform and occipital face areas of either the right or left hemisphere, but not in the right posterior superior temporal sulcus. The patients also showed some residual capabilities for facial discrimination with normal performance on the Benton Facial Recognition Test, but impaired performance on more complex tasks of facial discrimination. We conclude that fMRI can demonstrate residual processing of facial identity in acquired prosopagnosia, that this adaptation can occur in the same structures that show similar processing in healthy subjects, and further, that this adaptation may be related to behavioral indices of face perception.

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With the increasing sophistication and ubiquity of the Internet, behavioral research is on the cusp of a revolution that will do for population sampling what the computer did for stimulus control and measurement. It remains a common assumption, however, that data from self-selected Web samples must involve a trade-off between participant numbers and data quality. Concerns about data quality are heightened for performance-based cognitive and perceptual measures, particularly those that are timed or that involve complex stimuli. In experiments run with uncompensated, anonymous participants whose motivation for participation is unknown, reduced conscientiousness or lack of focus could produce results that would be difficult to interpret due to decreased overall performance, increased variability of performance, or increased measurement noise. Here, we addressed the question of data quality across a range of cognitive and perceptual tests. For three key performance metrics-mean performance, performance variance, and internal reliability-the results from self-selected Web samples did not differ systematically from those obtained from traditionally recruited and/or lab-tested samples. These findings demonstrate that collecting data from uncompensated, anonymous, unsupervised, self-selected participants need not reduce data quality, even for demanding cognitive and perceptual experiments.

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Whether a single perceptual process or separate and possibly independent processes support facial identity and expression recognition is unclear. We used a morphed-face discrimination test to examine sensitivity to facial expression and identity information in patients with occipital or temporal lobe damage, and structural and functional MRI to correlate behavioral deficits with damage to the core regions of the face-processing network. We found selective impairments of identity perception in two patients with right inferotemporal lesions and two prosopagnosic patients with damage limited to the anterior temporal lobes. Of these four patients one exhibited damage to the right fusiform and occipital face areas, while the remaining three showed sparing of these regions. Thus impaired identity perception can occur with damage not only to the fusiform and occipital face areas, but also to other medial occipitotemporal structures that likely form part of a face recognition network. Impaired expression perception was seen in the fifth patient with damage affecting the face-related portion of the posterior superior temporal sulcus. This subject also had difficulty in discriminating identity when irrelevant variations in expression needed to be discounted. These neuropsychological and neuroimaging data provide evidence to complement models which address the separation of expression and identity perception within the face-processing network.

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Theories of embodied cognition propose that recognizing facial expressions requires visual processing followed by simulation of the somatovisceral responses associated with the perceived expression. To test this proposal, we targeted the right occipital face area (rOFA) and the face region of right somatosensory cortex (rSC) with repetitive transcranial magnetic stimulation (rTMS) while participants discriminated facial expressions. rTMS selectively impaired discrimination of facial expressions at both sites but had no effect on a matched face identity task. Site specificity within the rSC was demonstrated by targeting rTMS at the face and finger regions while participants performed the expression discrimination task. rTMS targeted at the face region impaired task performance relative to rTMS targeted at the finger region. To establish the temporal course of visual and somatosensory contributions to expression processing, double-pulse TMS was delivered at different times to rOFA and rSC during expression discrimination. Accuracy dropped when pulses were delivered at 60-100 ms at rOFA and at 100-140 and 130-170 ms at rSC. These sequential impairments at rOFA and rSC support embodied accounts of expression recognition as well as hierarchical models of face processing. The results also demonstrate that nonvisual cortical areas contribute during early stages of expression processing.

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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.

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Developmental prosopagnosia is characterized by severely impaired face recognition. Individuals with this disorder, which often runs in families, have no history of brain damage and intact early visual processing systems. Recent research has also demonstrated that many developmental prosopagnosics have normal or relatively good object recognition, indicating that their impairments are not the result of deficits to a unitary visual recognition mechanism. To investigate the nature of the impaired mechanisms, extensive testing was done on an individual with especially pure face processing deficits. The results ruled out all extant explanations of prosopagnosia except one that proposed that faces are recognized by a content-specific face processing mechanism. fMRI and MEG studies show that there are a variety of neural profiles in developmental prosopagnosia, which is consistent with behavioral studies demonstrating that it is a heterogeneous disorder.

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We tested functional activation for faces in patient D.F., who following acquired brain damage has a profound deficit in object recognition based on form (visual form agnosia) and also prosopagnosia that is undocumented to date. Functional imaging demonstrated that like our control observers, D.F. shows significantly more activation when passively viewing face compared to scene images in an area that is consistent with the fusiform face area (FFA) (p < 0.01). Control observers also show occipital face area (OFA) activation; however, whereas D.F.'s lesions appear to overlap the OFA bilaterally. We asked, given that D.F. shows FFA activation for faces, to what extent is she able to recognize faces? D.F. demonstrated a severe impairment in higher level face processing--she could not recognize face identity, gender or emotional expression. In contrast, she performed relatively normally on many face categorization tasks. D.F. can differentiate faces from non-faces given sufficient texture information and processing time, and she can do this is independent of color and illumination information. D.F. can use configural information for categorizing faces when they are presented in an upright but not a sideways orientation and given that she also cannot discriminate half-faces she may rely on a spatially symmetric feature arrangement. Faces appear to be a unique category, which she can classify even when she has no advance knowledge that she will be shown face images. Together, these imaging and behavioral data support the importance of the integrity of a complex network of regions for face identification, including more than just the FFA--in particular the OFA, a region believed to be associated with low-level processing.

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For more than 35 years, researchers have debated whether face recognition is carried out by face-specific mechanisms or whether it involves more general mechanisms that are also used for objects. Prosopagnosic patients have furnished powerful evidence for face-specific mechanisms. Yet for each case that has been tested there have always been several untested alternative explanations that could account for the case. As such, each of these individuals has not been sufficiently tested to provide conclusive evidence for face-specific processes. Here we make a stronger argument with a single case of severe developmental prosopagnosia by exhaustively addressing all extant alternatives. We reject each in turn and thus eliminate all alternative accounts. Because this case is developmental in etiology the results also indicate that face recognition involves developmental mechanisms different from those producing other visual recognition mechanisms.

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Developmental prosopagnosia is a lifelong impairment in face recognition despite normal low-level visual processing. Here we used magnetoencephalography (MEG) to examine the M170 response, a component occurring approximately 170 ms after stimulus onset, in a group of five developmental prosopagnosics. In normal subjects, the M170 is "face-selective", with a consistently higher amplitude to faces than to a wide variety of other visual stimulus categories; the N170, a component recorded using event-related potentials (ERP) and thought to be analogous to the M170, also shows this "face selectivity". Two previous ERP studies with developmental prosopagnosics have found attenuation or absence of face selectivity in the N170 response of these subjects [Bentin, S., Deouell, L. Y., and Soroker, N. (1999). Selective visual streaming in face recognition: Evidence from developmental prosopagnosia. Neuroreport, 10, 823-827; Kress, T., and Daum, I. (2003). Event-related potentials reflect impaired face recognition in patients with congenital prosopagnosia. Neuroscience Letters, 352, 133-136]. Three of our developmental prosopagnosic group showed this non-selective pattern at the M170 while the remaining two prosopagnosics were indistinguishable from normal controls. Thus, impaired face recognition is not necessarily correlated with an absence of the "face-selective" M170. Furthermore, ERP recordings collected simultaneously in the two developmental prosopagnosics with seemingly selective M170s also showed N170s within the same normal selective range, demonstrating that the face-selective signals found with MEG are not due to differences between MEG and ERP. While the presence of face selectivity at these neurophysiological markers is insufficient for predicting normal behavioral performance with faces, it could help to distinguish different classes of face recognition deficits.

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A central question in cognitive neuroscience is whether mechanisms exist that are specialized for particular domains. One of the most commonly cited examples of a domain-specific competence is the human ability to recognize upright faces. However, according to a widely discussed alternative hypothesis, face recognition is instead performed by mechanisms specialized for processing any object class for which an individual has expertise. Faces, according to this domain-general hypothesis, are just one example of an expert class. Nonface object expertise has been intensively investigated using a training procedure involving an artificial stimulus class known as greebles. A key prediction of this hypothesis is that individuals with face recognition impairments will also have impairments with other categories that control subjects have expertise with. Our results show that a man with severe prosopagnosia performed normally throughout the standard greeble training procedure. These findings indicate that face recognition and greeble recognition rely on separate mechanisms.

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The Benton Facial Recognition Test is used for clinical and research purposes, but evidence suggests that it is possible to pass the test with impaired face discrimination abilities. The authors tested 11 patients with developmental prosopagnosia using this test, and a majority scored in the normal range. Consequently, scores in the normal range should be interpreted cautiously, and testing should always be supplemented by other face tests.

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In the leading model of face perception, facial identity and facial expressions of emotion are recognized by separate mechanisms. In this report, we provide evidence supporting the independence of these processes by documenting an individual with severely impaired recognition of facial identity yet normal recognition of facial expressions of emotion. NM, a 40-year-old prosopagnosic, showed severely impaired performance on five of six tests of facial identity recognition. In contrast, she performed in the normal range on four different tests of emotion recognition. Because the tests of identity recognition and emotion recognition assessed her abilities in a variety of ways, these results provide solid support for models in which identity recognition and emotion recognition are performed by separate processes.

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This review of developmental disorders of vision focuses on only a few of the many disorders that disrupt visual development. Given the enormity of the human visual system in the primate brain and complexity of visual development, however, there are likely hundreds or thousands of types of disorders affecting high-level vision. The rapid progress seen in developmental dyslexia and WMS demonstrates the possibilities and difficulties inherent in researching such disorders, and the authors hope that similar progress will be made for congenital prosopagnosia and other disorders in the near future.

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The Warrington Recognition Memory for Faces (RMF) and the Benton Facial Recognition Test (BFRT) are commercially available tests that are commonly used by clinicians and cognitive neuropsychologists to evaluate unfamiliar face recognition. Yet, it is not clear that a normal score on either instrument demonstrates normal unfamiliar face recognition. Because the RMFs stimuli contain abundant non-internal facial feature information, subjects may be able to score in the normal range without using internal facial features. On the BFRT, subjects commonly rely on feature matching strategies using the hairline and eyebrows rather than recognizing the facial configuration. To test whether these routes to recognition can support normal performance, normal subjects were tested with versions of the RMF and the BFRT in which the faces had been painted over in a way that prevented the operation of some of the procedures normally involved with face recognition. Even though these modifications removed all of the internal feature information in the RMF, many subjects scored in the normal range, and despite precluding the use of configural processing in the BFRT, many of the scores were in the normal range. As a result, it is apparent that normal scores on these tests do not demonstrate normal unfamiliar face recognition and so clinicians should be cautious in interpreting scores in the normal range. Finally, these results place in question models supported by dissociations involving normal performance on these tests.

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We report the results of tests investigating the recognition of faces, places, and objects in a developmental agnosic, because dissociations of visual recognition in developmental agnosics provide insight into the separable procedures performing recognition and the developmental origins of these procedures. TA is a software engineer in his early 40s with developmental prosopagnosia. He performs normally on tests of low-level vision, and he names objects at the basic level normally. In order to compare his recognition abilities for different classes, we have presented him with a famous landmarks test, a famous faces test, and old/new discriminations involving unfamiliar faces, houses, natural landscapes, cars, horses, guns, sunglasses, and tools. He was impaired on the face recognition tests, but performed normally on the place recognition tests. He also showed severe impairments with horses and cars, borderline impairments with guns and sunglasses, and normal performance with tools. These results indicate that the developmental processes that assemble the procedures used for face recognition and certain types of object recognition are separate from those processes that produce the procedures used for place recognition.

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