Binocular rivalry reveals differential face processing in congenital prosopagnosia.

Congenital Prosopagnosia (CP) is an innate impairment in face perception with heterogeneous characteristics. It is still unclear if and to what degree holistic processing of faces is disrupted in CP. Such disruption would be expected to lead to a focus on local features of the face. In this study, we used binocular rivalry (BR) to implicitly measure face perception in conditions that favour holistic or local processing. The underlying assumption is that if stimulus saliency affects the perceptual dominance of a given stimulus in BR, one can deduce how salient a stimulus is for a given group (here: participants with and without CP) based on the measured perceptual dominance. A further open question is whether the deficit in face processing in CP extends to the processing of the facial display of emotions. In experiment 1, we compared predominance of upright and inverted faces displaying different emotions (fearful, happy, neutral) vs. houses between participants with CP (N = 21) and with normal face perception (N = 21). The results suggest that CP observers process emotions in faces automatically but rely more on local features than controls. The inversion of faces, which is supposed to disturb holistic processing, affected controls in a more pronounced way than participants with CP. In experiment 2, we introduced the Thatcher effect in BR by inverting the eye and mouth regions of the presented faces in the hope of further increasing the effect of face inversion. However, our expectations were not borne out by the results. Critically, both experiments showed that inversion effects were more pronounced in controls than in CP, suggesting that holistic face processing is less relevant in CP. We find BR to be a useful implicit test for assessing visual processing specificities in neurological participants.

Alcohol Use Predicts Face Perception Impairments and Difficulties in Face Recognition.

Background: Risky alcohol use is related to a variety of cognitive impairments, including memory and visuo-perceptual difficulties. Remarkably, no prior work has assessed whether usage of alcohol can predict difficulties perceiving facial identity. Objectives: Therefore, this study aimed to investigate whether riskier alcohol consumption predicted impairments in face perception and self-reported difficulties in face recognition. Results: Participants (N = 239, male = 77) were over 18 years old and had normal or corrected-to-normal vision. Alcohol use was assessed using the Alcohol Use Disorder Identification Test (AUDIT), while face recognition difficulties were determined by the 20-item Prosopagnosia Index questionnaire (PI20). A subsample of participants (N = 126, male = 51) completed the Cambridge Face Perception task (CFPT) to assess their face perception ability. Multiple linear regressions showed significant models of prediction on both face perception and face recognition when considering AUDIT score and age as predictors. Conclusion: This study suggested, for the first time, that risky alcohol use predicts both poorer visuo-perceptual processing for faces and self-reported difficulties in face recognition.

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.

Investigating the Influence of Autism Spectrum Traits on Face Processing Mechanisms in Developmental Prosopagnosia.

Autism traits are common exclusionary criteria in developmental prosopagnosia (DP) studies. We investigated whether autism traits produce qualitatively different face processing in 43 DPs with high vs. low autism quotient (AQ) scores. Compared to controls (n = 27), face memory and perception were similarly deficient in the high- and low-AQ DPs, with the high-AQ DP group additionally showing deficient face emotion recognition. Task-based fMRI revealed reduced occipito-temporal face selectivity in both groups, with high-AQ DPs additionally demonstrating decreased posterior superior temporal sulcus selectivity. Resting-state fMRI showed similar reduced face-selective network connectivity in both DP groups compared with controls. Together, this demonstrates that high- and low-AQ DP groups have very similar face processing deficits, with additional facial emotion deficits in high-AQ DPs.

Not so fast! Response times in the computerized Benton Face Recognition Test may not reflect face recognition ability.

Response times (RTs) are commonly used to assess cognitive abilities, though it is unclear whether face processing RTs predict recognition ability beyond accuracy. In the current study, we examined accuracy and RT on a widely used face matching assessment modified to collect meaningful RT data, the computerized Benton Facial Recognition Test (BFRT-c), and measured whether RTs predicted face recognition ability and developmental prosopagnosia (DP) vs. control group membership. 62 controls and 36 DPs performed the BFRT-c as well as validated measures of face recognition ability: the Cambridge Face Memory Test (CFMT) and a Famous Faces Memory Test (FFMT). In controls, BFRT-c accuracy robustly predicted CFMT (r = .49, p < .001), FFMT (r = .43, p < .001), and a CFMT-FFMT composite (r = .54, p < .001), whereas BFRT-c RT was not significantly associated with these measures (all r's .21). We also found that BFRT-c accuracy significantly differed between DPs and controls, but RT failed to differentiate the groups.

Face specific inversion effects provide evidence for two subtypes of developmental prosopagnosia.

Many studies have attempted to identify the perceptual underpinnings of developmental prosopagnosia (DP). The majority have focused on whether holistic and configural processing mechanisms are impaired in DP. However, previous work suggests that there is substantial heterogeneity in holistic and configural processing within the DP population; further, there is disagreement as to whether any deficits are face-specific or reflect a broader perceptual deficit. This study used a data-driven approach to examine whether there are systematic patterns of variability in DP that reflect different underpinning perceptual deficits. A group of individuals with DP (N = 37) completed a cognitive battery measuring holistic/configural and featural processing in faces and non-face objects. A two-stage cluster analysis on data from the Cambridge Face Perception Test identified two subgroups of DPs. Across several tasks, the first subgroup (N = 21) showed typical patterns of holistic/configural processing (measured via inversion effects); the second (N = 16) was characterised by reduced or abolished inversion effects compared to age-matched control participants (N = 91). The subgroups did not differ on tasks measuring upright face matching, object matching, non-face holistic processing, or composite effects. These findings indicate two separable pathways to face recognition impairment, one characterised by impaired configural processing and the other potentially by impaired featural processing. Comparisons to control participants provide some preliminary evidence that the deficit in featural processing may extend to some non-face stimuli. Our results demonstrate the utility of examining both the variability between and consistency across individuals with DP as a means of illuminating our understanding of face recognition in typical and atypical populations.

Anatomical and neurophysiological basis of face recognition.

Face recognition is a highly developed and efficient human function that involves multiple neural networks. A main pathway links the occipital cortex, where an occipital face area (OFA) has been identified, to a fusiform face area (FFA) in the fusiform gyrus, which plays a critical role in face recognition. This core pathway deals with invariant aspects of the face. Another pathway, including the superior temporal sulcus, is involved in the perception of more changeable aspects of the face such as gaze orientation, face expression and lip movements. It has been defined by some authors as a "third pathway of visual recognition", i.e. a lateral pathway in addition to the "what" and "where" pathways. It deals with sociocognitive aspects of face perception. Many other accessory functional systems are connected to the core system of visual recognition to act in concert with it: the intraparietal sulcus (for the management of spatial attention), the primary auditory cortex (prelexical perception of speech), the amygdala, the insula and the limbic system (perception of emotions), the anterior temporal pole (access to the identity of the individual, his name, biographical information), etc. Functional brain imaging has made remarkable progress in the understanding of face perception, which in the early years was limited to the description of single cases of brain-damaged patients. This progress has made it possible to better analyse the many face recognition disorders, sometimes subtle, other times confusing, observed in human pathology.

Comparing the sensitivity of face matching assessments to detect face perception impairments.

Numerous neurological, developmental, and psychiatric conditions demonstrate impaired face recognition, which can be socially debilitating. These impairments can be caused by either deficient face perception or face memory mechanisms. Though there are well-validated, sensitive measures of face memory impairments, it currently remains unclear which assessments best measure face perception impairments. A sensitive, validated face perception measure could help with diagnosing causes of face recognition deficits and be useful in characterizing individual differences in unimpaired populations. Here, we compared the computerized Benton Face Recognition Test (BFRT-c) and Cambridge Face Perception Test (CFPT) in their ability to differentiate developmental prosopagnosics (DPs, N = 30) and age-matched controls (N = 30). Participants completed the BFRT-c, CFPT, and two additional face perception assessments: the University of Southern California Face Perception Test (USCFPT) and a novel same/different face matching test (SDFMT). Participants were also evaluated on objective and subjective face recognition tasks including the Cambridge Face Memory Test, famous faces test, and Prosopagnosia Index-20. We performed a logistic regression with the perception tests predicting DP vs. control group membership and used multiple linear regressions to predict continuous objective and subjective face recognition memory. Our results show that the BFRT-c performed as well as, if not better than, the CFPT, and that both tests clearly outperformed the USCFPT and SDFMT. Further, exploratory analyses revealed that face lighting-change conditions better predicted DP group membership and face recognition abilities than viewpoint-change conditions. Together, these results support the combined use of the BFRT-c and CFPT to best assess face perception impairments.

Spatial Integration in Normal Face Processing and Its Breakdown in Congenital Prosopagnosia.

Congenital prosopagnosia (CP), a life-long impairment in face processing that occurs in the absence of any apparent brain damage, provides a unique model in which to explore the psychological and neural bases of normal face processing. The goal of this review is to offer a theoretical and conceptual framework that may account for the underlying cognitive and neural deficits in CP. This framework may also provide a novel perspective in which to reconcile some conflicting results that permits the expansion of the research in this field in new directions. The crux of this framework lies in linking the known behavioral and neural underpinnings of face processing and their impairments in CP to a model incorporating grid cell-like activity in the entorhinal cortex. Moreover, it stresses the involvement of active, spatial scanning of the environment with eye movements and implicates their critical role in face encoding and recognition. To begin with, we describe the main behavioral and neural characteristics of CP, and then lay down the building blocks of our proposed model, referring to the existing literature supporting this new framework. We then propose testable predictions and conclude with open questions for future research stemming from this model.

[A case suspected of Alzheimer type dementia showing multimodal (face and voice) person recognition disorder from face and voice].

A 90-year-old woman presented with a multimodal (face and voice) person recognition disorder. Although she had moderate general cognitive impairment, her visual cognitive capacity, other than face recognition, was well preserved. She could identify the faces and voices of family members but could not recall the names and voices of relatives whom she met infrequently, famous individuals, or the medical staff. She could remember the first names and some information about prominent individuals when supplied with their surnames. Therefore, we thought that her person-specific semantic memory was intact but she was unable to access it through their faces and voices. MRI revealed predominantly right-sided bilateral anterior temporal lobe and hippocampal atrophy. SPECT images showed decreased blood flow in the bilateral anterior temporal lobes and inferior parietal lobule (heavily and predominantly right-sided), right posterior cingulate gyrus, and precuneus. Progressive person recognition disorder or prosopagnosia has been considered a right temporal variant of frontotemporal lobar degeneration because abnormal behaviors and psychiatric symptoms frequently coexist. However, no such symptoms were observed in this case, therefore we suspected dementia of the Alzheimer type.

People have modest, not good, insight into their face recognition ability: a comparison between self-report questionnaires.

Whether people have insight into their face recognition ability has been intensely debated in recent studies using self-report measures. Although some studies showed people's good insight, other studies found the opposite. The discrepancy might be caused by the difference in the questionnaire used and/or the bias induced using an extreme group such as suspected prosopagnosics. To resolve this issue, we examined the relationship between the two representative self-report face recognition questionnaires (Survey, N = 855) and then the extent to which the questionnaires differ in their relationship with face recognition performance (Experiment, N = 180) in normal populations, which do not include predetermined extreme groups. We found a very strong correlation (r = 0.82), a dominant principal component (explains > 90% of the variance), and comparable reliability between the questionnaires. Although these results suggest a strong common factor underlying them, the residual variance is not negligible (33%). Indeed, the follow-up experiment showed that both questionnaires have significant but moderate correlations with actual face recognition performance, and that the correlation was stronger for the Kennerknecht's questionnaire (r = - 0.38) than for the PI20 (r = - 0.23). These findings not only suggest people's modest insight into their face recognition ability, but also urge researchers and clinicians to carefully assess whether a questionnaire is suitable for estimating an individual's face recognition ability.

The discrimination of facial sex in developmental prosopagnosia.

Developmental prosopagnosia (DP) is a neurodevelopmental condition characterised by difficulties recognising and discriminating faces. It is currently unclear whether the perceptual impairments seen in DP are restricted to identity information, or also affect the perception of other facial characteristics. To address this question, we compared the performance of 17 DPs and matched controls on two sensitive sex categorisation tasks. First, in a morph categorisation task, participants made binary decisions about faces drawn from a morph continuum that blended incrementally an average male face and an average female face. We found that judgement precision was significantly lower in the DPs than in the typical controls. Second, we used a sex discrimination task, where female or male facial identities were blended with an androgynous average face. We manipulated the relative weighting of each facial identity and the androgynous average to create four levels of signal strength. We found that DPs were significantly less sensitive than controls at each level of difficulty. Together, these results suggest that the visual processing difficulties in DP extend beyond the extraction of facial identity and affects the extraction of other facial characteristics. Deficits of facial sex categorisation accord with an apperceptive characterisation of DP.

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.

The domain-specificity of face matching impairments in 40 cases of developmental prosopagnosia.

A prevailing debate in the psychological literature concerns the domain-specificity of the face recognition system, where evidence from typical and neurological participants has been interpreted as evidence that faces are "special". Although several studies have investigated the same question in cases of developmental prosopagnosia, the vast majority of this evidence has recently been discounted due to methodological concerns. This leaves an uncomfortable void in the literature, restricting our understanding of the typical and atypical development of the face recognition system. The current study addressed this issue in 40 individuals with developmental prosopagnosia, completing a sequential same/different face and biological (hands) and non-biological (houses) object matching task, with upright and inverted conditions. Findings support domain-specific accounts of face-processing for both hands and houses: while significant correlations emerged between all the object categories, no condition correlated with performance in the upright faces condition. Further, a categorical analysis demonstrated that, when face matching was impaired, object matching skills were classically dissociated in six out of 15 individuals (four for both categories). These findings provide evidence about domain-specificity in developmental disorders of face recognition, and present a theoretically-driven means of partitioning developmental prosopagnosia.

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.

Atypical holistic processing of facial identity and expression in a case of acquired prosopagnosia.

Typical face perception is mediated by holistic processing (i.e., the simultaneous integration of face parts into a whole representation). People with Acquired Prosopagnosia (AP), who have lost the ability to recognise faces after a brain lesion, should thus show atypical holistic coding. Our aim is to use the composite-face effect (CFE) as a measure of holistic processing in ST, a 48-year-old woman with AP but normal recognition of facial expressions of emotions, and matched healthy control participants. Two experiments examining the CFE for identity (Experiment 1) and for expression of emotions (Experiment 2) were conducted. Contrary to controls, in both experiments, ST showed an atypical (i.e., reversed) CFE, thus suggesting altered holistic mechanisms affecting both components of perceptual judgement. Results also suggest that normal facial expression recognition is achievable even with holistic processing difficulties, possibly through compensatory, part-based, mechanisms.

The good, the bad, and the average: Characterizing the relationship between face and object processing across the face recognition spectrum.

Face recognition skills vary considerably both in the normal population and in various clinical groups, and understanding the cognitive mechanisms contributing to this variability is important. In the present study, we investigate whether a group of good face recognizers (high performers; HPs) perform qualitatively differently from a control group on tests of face, object and word recognition, and also compare them to a group of developmental prosopagnosics (DPs). Through a series of experiments, we (i) examine whether HPs are better than control subjects in face and object recognition, (ii) investigate if any dissociations among face, object, and word processing tasks can be demonstrated in the HPs, and (iii) compare the performance of the HPs to a group of poor face recognizers namely a group of DPs. Data from this DP group have previously been reported, but the analyses presented here are new. We find that HPs were significantly better than matched control subjects on tests of face and object recognition including a reading task, but they did not show significantly larger inversion effects on typical tests of face processing (the CFMT and the CFPT). There was no evidence of dissociations between face and object processing in the HPs when compared to controls, indicating superior performance across visual domains. In the DP group, however, we found significant dissociations between face and object recognition performance on a group level, indicating that face processing is disproportionally affected. On this basis, we propose that superior face processing in HPs rely on more general cognitive or perceptual processes shared with object processing. Hence, while face processing in DPs seems qualitatively different from the normal population, there is no such difference between average and high performing face recognizers. Thus, what underlies superior face processing in HPs might also underlie their superior performance with other stimulus classes and might be conceived as a general factor in the visual domain, a VG-factor, akin to the G factor in intelligence.

Is developmental prosopagnosia best characterised as an apperceptive or mnemonic condition?

Traditionally, developmental prosopagnosia (DP) has been thought of as an apperceptive condition that hinders individuals' ability to encode face structure. However, several authors have recently raised the possibility that many DPs may be able to form accurate percepts, but be unable to maintain those percepts over time. The present study sought to distinguish these possibilities. In our first experiment 16 DPs and 22 typical controls completed a delayed match-to-sample task with face and car stimuli, with a retention interval of 1-second (low demand) or 6-seconds (high demand). As expected, the participants with DP were worse than the controls at face matching, and were disproportionately impaired at matching faces relative to cars. However, the relative degree of impairment seen in the DPs did not interact with retention interval; they exhibited similar levels of impairment when matching faces with 1- and 6-second delays. Next, we compared the performance of 72 DPs and 54 typical controls on the Cambridge Face Perception Test (CFPT), a task that measures face perception ability in a way that minimises the memory demands. As expected, we found that the DPs were impaired at the group level. This difference was not attributable to a few individuals with an apperceptive profile; rather we found evidence that the distribution of CFPT scores seen in the DP sample was shifted relative to that of typical controls. Some heterogeneity is likely in any neurodevelopmental population, and DP is no different. Generally, however, these findings suggest that selective STFM impairment may be relatively uncommon in this population. Instead, deficits of perceptual encoding may play a larger role in DP than currently acknowledged.

Developmental prosopagnosia with concurrent topographical difficulties: A case report and virtual reality training programme.

Several neuropsychological case studies report brain-damaged individuals with concurrent impairments in face recognition (i.e., prosopagnosia) and topographical orientation. Recently, individuals with a developmental form of topographical disorientation have also been described, and several case reports of individuals with developmental prosopagnosia provide anecdotal evidence of concurrent navigational difficulties. Clearly, the co-occurrence of these difficulties can exacerbate the negative psychosocial consequences associated with each condition. This paper presents the first detailed case report of an individual (FN) with developmental prosopagnosia alongside difficulties in topographical orientation. FN's performance on an extensive navigational battery indicated that she primarily has difficulties in the formation and retrieval of cognitive maps. We then evaluated the effectiveness of a short-term virtual reality training programme and found that she is able to form a cognitive map of a particular environment following intense overlearning. Surprisingly, FN's performance on a face recognition task also improved following training. While the latter finding was unexpected and requires further exploration, the training programme reported here may help to alleviate some of the compounded negative psychosocial consequences that are associated with difficulties in finding both locations and people.

Tests of whole upright face processing in prosopagnosia: A literature review.

Prosopagnosia refers to an acquired or developmental deficit in face recognition. This neuropsychological impairment has received increasing attention over the last decade, in particular because of an increased scientific interest in developmental prosopagnosia. Studies investigating prosopagnosia have used a variety of different clinical and experimental tests to assess face processing abilities. With such a large variety of assessment methods available, test selection can be challenging. Some previous works have aimed to provide an overview of tests used to diagnose prosopagnosia. However, no overview that is based on a structured review of the literature is available. We review the literature to identify tests that have been used to assess the processing of whole upright faces in acquired and developmental prosopagnosia over the last five years (2013-2017). We not only review tests that have been used for diagnostic purposes, but also tests that have been used for experimental purposes. Tests are categorised according to i) their experimental designs and, ii) the stage of face processing that they assess. On this basis, we discuss considerations regarding test designs for future studies. A visual illustration providing a structured overview of paradigms available for testing the processing of whole upright faces is provided. This visual illustration can be used to inform test selection when designing a study and to apply a structured approach to interpreting findings from the literature. The different approaches to assessment of face processing in prosopagnosia have been necessary and fruitful in generating data and hypotheses about the cause of face processing deficits. However, impairments at different levels of face processing have often been interpreted as reflecting a deficit in the recognition stage of face processing. Based on the data now available on prosopagnosia, we advocate for a more structured approach to assessment, which may facilitate a better understanding of the key deficits in prosopagnosia and of the level(s) of face processing that are impaired.