Familiarity enhances functional connectivity between visual and nonvisual regions of the brain during natural viewing.

We explored the neural correlates of familiarity with people and places using a naturalistic viewing paradigm. Neural responses were measured using functional magnetic resonance imaging, while participants viewed a movie taken from Game of Thrones. We compared inter-subject correlations and functional connectivity in participants who were either familiar or unfamiliar with the TV series. Higher inter-subject correlations were found between familiar participants in regions, beyond the visual brain, that are typically associated with the processing of semantic, episodic, and affective information. However, familiarity also increased functional connectivity between face and scene regions in the visual brain and the nonvisual regions of the familiarity network. To determine whether these regions play an important role in face recognition, we measured responses in participants with developmental prosopagnosia (DP). Consistent with a deficit in face recognition, the effect of familiarity was significantly attenuated across the familiarity network in DP. The effect of familiarity on functional connectivity between face regions and the familiarity network was also attenuated in DP. These results show that the neural response to familiarity involves an extended network of brain regions and that functional connectivity between visual and nonvisual regions of the brain plays an important role in the recognition of people and places during natural viewing.

Prosopagnosia does not abolish other-race effects.

Healthy observers recognize more accurately same-than other-race faces (i.e., the Same-Race Recognition Advantage - SRRA) but categorize them by race more slowly than other-race faces (i.e., the Other-Race Categorization Advantage - ORCA). Several fMRI studies reported discrepant bilateral activations in the Fusiform Face Area (FFA) and Occipital Face Area (OFA) correlating with both effects. However, due to the very nature and limits of fMRI results, whether these face-sensitive regions play an unequivocal causal role in those other-race effects remains to be clarified. To this aim, we tested PS, a well-studied pure case of acquired prosopagnosia with lesions encompassing the left FFA and the right OFA. PS, healthy age-matched and young adults performed two recognition and three categorization by race tasks, respectively using Western Caucasian and East Asian faces normalized for their low-level properties with and without-external features, as well as in naturalistic settings. As expected, PS was slower and less accurate than the controls. Crucially, however, the magnitudes of her SRRA and ORCA were comparable to the controls in all the tasks. Our data show that prosopagnosia does not abolish other-race effects, as an intact face system, the left FFA and/or right OFA are not critical for eliciting the SRRA and ORCA. Race is a strong visual and social signal that is encoded in a large neural face-sensitive network, robustly tuned for processing same-race faces.

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.

Multi-Item Discriminability Pattern to Faces in Developmental Prosopagnosia Reveals Distinct Mechanisms of Face Processing.

Previous studies have shown that individuals with developmental prosopagnosia (DP) show specific deficits in face processing. However, the mechanism underlying the deficits remains largely unknown. One hypothesis suggests that DP shares the same mechanism as normal population, though their faces processing is disproportionally impaired. An alternative hypothesis emphasizes a qualitatively different mechanism of DP processing faces. To test these hypotheses, we instructed DP and normal individuals to perceive faces and objects. Instead of calculating accuracy averaging across stimulus items, we used the discrimination accuracy for each item to construct a multi-item discriminability pattern. We found DP's discriminability pattern was less similar to that of normal individuals when perceiving faces than perceiving objects, suggesting that DP has qualitatively different mechanism in representing faces. A functional magnetic resonance imaging study was conducted to reveal the neural basis and found that multi-voxel activation patterns for faces in the right fusiform face area and occipital face area of DP were deviated away from the mean activation pattern of normal individuals. Further, the face representation was more heterogeneous in DP, suggesting that deficits of DP may come from multiple sources. In short, our study provides the first direct evidence that DP processes faces qualitatively different from normal population.

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.

Progress in perceptual research: the case of prosopagnosia.

Prosopagnosia is an impairment in the ability to recognize faces and can be acquired after a brain lesion or occur as a developmental variant. Studies of prosopagnosia make important contributions to our understanding of face processing and object recognition in the human visual system. We review four areas of advances in the study of this condition in recent years. First are issues surrounding the diagnosis of prosopagnosia, including the development and evaluation of newer tests and proposals for diagnostic criteria, especially for the developmental variant. Second are studies of the structural basis of prosopagnosia, including the application of more advanced neuroimaging techniques in studies of the developmental variant. Third are issues concerning the face specificity of the defect in prosopagnosia, namely whether other object processing is affected to some degree and in particular the status of visual word processing in light of recent predictions from the "many-to-many hypothesis". Finally, there have been recent rehabilitative trials of perceptual learning applied to larger groups of prosopagnosic subjects that show that face impairments are not immutable in this condition.

Multimodal face and voice recognition disorders in a case with unilateral right anterior temporal lobe atrophy.

OBJECTIVE: Familiar face recognition disorders are often observed in patients with lesions of the right anterior temporal lobe (ATL). It is not clear, however, if this defect must be considered as a form of associative prosopagnosia, or as a multimodal (face and voice) people recognition disorder, because voice recognition is rarely examined in these patients. The most appropriate manner of solving this problem could consist in evaluating, in one or more patients with right ATL lesions, recognition disorders through face and voice of the same well known people. METHODS: The 'Famous People Recognition Battery' (FPRB), in which the same 40 persons (very well-known at the national level) should be identified through face and voice recognition, was used to clarify this issue. The FPRB was administered to a 56-year-old woman (BM) who complained, as early sign of a fronto-temporal degeneration, of familiar people recognition defects in a context of relatively intact cognitive functions. RESULTS: On the FPRB, BM showed a severe defect of people recognition (familiarity judgement) and identification through face and voice, but not through personal name. Voxel-based morphometry showed a focal atrophy of the right ATL (temporo-polar cortex and anterior parts of perirhinal and entorhinal cortices). CONCLUSIONS: the present case report seems to show that a unilateral right ATL atrophy can lead to a multimodal people recognition disorder through face and voice, in the absence of recognition difficulties through personal name. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Face processing in a case of high functioning autism with developmental prosopagnosia.

The ability to "read" the information about facial identity, expressed emotions, and intentions is crucial for non­verbal social interaction. Neuroimaging and clinical studies consequently link face perception with fusiform gyrus (FG) and occipital face area (OFA) activity. Here we investigated face processing in an adult, patient PK, diagnosed with both high functioning autism spectrum disorder (ASD) and developmental prosopagnosia (DP). Both disorders have a significant impact on face perception and recognition, thus creating a unique neurodevelopmental condition. We used eye­tracking and functional magnetic resonance imaging (fMRI) method. Eye­tracking and fMRI results of PK were compared to results of control subjects. Patient PK showed atypical gaze­fixation strategy during face perception and typical patterns of brain activations in the FG and OFA. However, a significant difference between PK and control subjects was found in the left anterior superior temporal sulcus/middle temporal gyrus (aSTS/MTG). In PK the left aSTS/MTG was hypo­activated in comparison to the control subjects. Additionally, functional connectivity analysis revealed decreased inter­hemispheric connectivity between right and left aSTS/MTG in 'ASD and DP' patient during face recognition performance as compared to the control subjects. The lack of activity in the left aSTS/MTG observed in the case of the clinical subject, combined with the behavioral, eye­tracking, and neuropsychological results, suggests that impairment of the cognitive mechanism of face recognition involves higher level of processing. It seems to be related to insufficient access to semantic knowledge about the person when prompted by face stimuli.

The neural network for face recognition: Insights from an fMRI study on developmental prosopagnosia.

Face recognition is supported by collaborative work of multiple face-responsive regions in the brain. Based on findings from individuals with normal face recognition ability, a neural model has been proposed with the occipital face area (OFA), fusiform face area (FFA), and face-selective posterior superior temporal sulcus (pSTS) as the core face network (CFN) and the rest of the face-responsive regions as the extended face network (EFN). However, little is known about how these regions work collaboratively for face recognition in our daily life. Here we focused on individuals suffering developmental prosopagnosia (DP), a neurodevelopmental disorder specifically impairing face recognition, to shed light on the infrastructure of the neural model of face recognition. Specifically, we used a variant of global brain connectivity method to comprehensively explore resting-state functional connectivity (FC) among face-responsive regions in a large sample of DPs (N = 64). We found that both the FCs within the CFN and those between the CFN and EFN were largely reduced in DP. Importantly, the right OFA and FFA served as the dysconnectivity hubs within the CFN, i.e., FCs concerning these two regions within the CFN were largely disrupted. In addition, DPs' right FFA also showed reduced FCs with the EFN. Moreover, these disrupted FCs were related to DP's behavioral deficit in face recognition, with the FCs from the FFA to the anterior temporal lobe (ATL) and pSTS the most predictive. Based on these findings, we proposed a revised neural model of face recognition demonstrating the relatedness of interactions among face-responsive regions to face recognition.

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.

The cognitive and neural basis of developmental prosopagnosia.

Developmental prosopagnosia (DP) is a severe impairment of visual face recognition in the absence of any apparent brain damage. The factors responsible for DP have not yet been fully identified. This article provides a selective review of recent studies investigating cognitive and neural processes that may contribute to the face recognition deficits in DP, focusing primarily on event-related brain potential (ERP) measures of face perception and recognition. Studies that measured the face-sensitive N170 component as a marker of perceptual face processing have shown that the perceptual discrimination between faces and non-face objects is intact in DP. Other N170 studies suggest that faces are not represented in the typical fashion in DP. Individuals with DP appear to have specific difficulties in processing spatial and contrast deviations from canonical upright visual-perceptual face templates. The rapid detection of emotional facial expressions appears to be unaffected in DP. ERP studies of the activation of visual memory for individual faces and of the explicit identification of particular individuals have revealed differences between DPs and controls in the timing of these processes and in the links between visual face memory and explicit face recognition. These observations suggest that the speed and efficiency of information propagation through the cortical face network is altered in DP. The nature of the perceptual impairments in DP suggests that atypical visual experience with the eye region of faces over development may be an important contributing factor to DP.

Localization and patterns of Cerebral dyschromatopsia: A study of subjects with prospagnosia.

OBJECTIVE: Cerebral dyschromatopsia is sometimes associated with acquired prosopagnosia. Given the variability in structural lesions that cause acquired prosopagnosia, this study aimed to investigate the structural correlates of prosopagnosia-associated dyschromatopsia, and to determine if such colour processing deficits could also accompany developmental prosopagnosia. In addition, we studied whether cerebral dyschromatopsia is typified by a consistent pattern of hue impairments. METHODS: We investigated hue discrimination in a cohort of 12 subjects with acquired prosopagnosia and 9 with developmental prosopagnosia, along with 42 matched controls, using the Farnsworth-Munsell 100-hue test. RESULTS: We found impaired hue discrimination in six subjects with acquired prosopagnosia, five with bilateral and one with a unilateral occipitotemporal lesion. Structural MRI analysis showed maximum overlap of lesions in the right and left lingual and fusiform gyri. Fourier analysis of their error scores showed tritanopic-like deficits and blue-green impairments, similar to tendencies displayed by the healthy controls. Three subjects also showed a novel fourth Fourier component, indicating additional peak deficits in purple and green-yellow regions. No subject with developmental prosopagnosia had impaired hue discrimination. CONCLUSIONS: In our subjects with prosopagnosia, dyschromatopsia occurred in those with acquired lesions of the fusiform gyri, usually bilateral but sometimes unilateral. The dyschromatopsic deficit shows mainly an accentuation of normal tritatanopic-like tendencies. These are sometimes accompanied by additional deficits, although these could represent artifacts of the testing procedure.

Temporal lobe contribution to perceptual function: A tale of three patient groups.

There has been growing recognition of the contribution of medial and anterior temporal lobe structures to non-mnemonic functions, such as perception. To evaluate the nature of this contribution, we contrast the perceptual performance of three patient groups, all of whom have a perturbation of these temporal lobe structures. Specifically, we compare the profile of patients with focal hippocampal (HC) lesions, those with more extensive lesions to the medial temporal lobe (MTL) that include HC and perirhinal cortex (PrC), and those with congenital prosopagnosia (CP), whose deficit has been attributed to the disconnection of the anterior temporal lobe from more posterior structures. All participants completed a range of'oddity' tasks in which, on each trial, they determined which of four visual stimuli in a display was the'odd-one-out'. There were five stimulus categories including faces, scenes, objects (high and low ambiguity) and squares of different sizes. Comparisons were conducted separately for the HC, MTL and CP groups against their matched control groups and then the group data were compared to each other directly. The group profiles were easily differentiable. Whereas the HC group stood out for its difficulty in discriminating scenes and the CP group stood out for its disproportionate difficulty in discriminating faces with milder effects for scenes and high ambiguity objects, the MTL group evinced a more general discrimination deficit for faces, scenes and high ambiguity objects. The group differences highlight distinct profiles for each of the three groups and distinguish the signature perceptual impairments following more extended temporal lobe alterations. In the recent reconsideration of the role of the hippocampus and neocortex, Moscovitch and colleagues (Moscovitch et al., 2016) note that the medial temporal lobe structures play a role in non-mnemonic functions, such as perception, problem solving, decision-making and language. Here, we address this exact issue, specifically with respect to perception, and we dedicate this paper to Morris Moscovitch in recognition of his profound contribution to science, to his students and to his colleagues.

Unilateral left prosopometamorphopsia: a neuropsychological case study.

We describe a patient who suddenly developed prosopometamorphopsia after a childbirth; she claimed that the left half of well-known and unfamiliar faces looked distorted. Brain MR was normal, whereas SPECT showed hypoperfusion of the left infero-lateral occipital cortex. No visual recognition defects for objects or faces were present. In three matching tasks with half-faces (Experiment 1), chimeric faces (Experiment 2), or chimeric objects (Experiment 3), the patient was impaired only when she matched pairs of chimeric faces differing in their left half; the same results were obtained after 1 year. This is the first behavioural demonstration of selective chronic metamorphopsia for the left side of faces, and provides new insights for models of face processing.