Disentangling developmental prosopagnosia: A scoping review of terms, tools and topics.

The goal of this preregistered scoping review is to create an overview of the research on developmental prosopagnosia (DP). Through analysis of all empirical studies of DP in adults, we investigate 1) how DP is conceptualized and defined, 2) how individuals are classified with DP and 3) which aspects of DP are investigated in the literature. We reviewed 224 peer-reviewed studies of DP. Our analysis of the literature reveals that while DP is predominantly defined as a lifelong face recognition impairment in the absence of acquired brain injury and intellectual/cognitive problems, there is far from consensus on the specifics of the definition with some studies emphasizing e.g., deficits in face perception, discrimination and/or matching as core characteristics of DP. These differences in DP definitions is further reflected in the vast heterogeneity in classification procedures. Only about half of the included studies explicitly state how they classify individuals with DP, and these studies adopt 40 different assessment tools. The two most frequently studied aspects of DP are the role of holistic processing and the specificity of face processing, and alongside a substantial body of neuroimaging studies of DP, this paints a picture of a research field whose scientific interests and aims are rooted in cognitive neuropsychology and neuroscience. We argue that these roots - alongside the heterogeneity in DP definition and classification - may have limited the scope and interest of DP research unnecessarily, and we point to new avenues of research for the field.

Perceptual heterogeneity in developmental prosopagnosia is continuous, not categorical.

Developmental prosopagnosia (DP) is associated with considerable perceptual heterogeneity, though the nature of this heterogeneity and whether there are discrete subgroups versus continuous deficits remains unclear. Bennetts et al. (2022) recently found that holistic versus featural processing deficits distinguished discrete DP subgroups, but their sample was relatively small (N = 37), and subgroups were defined using a single task. To characterize perceptual heterogeneity in DPs more comprehensively, we administered a broad face perception battery to a large sample of 109 DPs and 134 controls, including validated measures of face matching (Cambridge Face Perception Test - CFPT, Computerized Benton Facial Recognition Test, Same/Different Face Matching Task), holistic processing (Part-Whole Task), and feature processing (Georges Task and Part-Whole part trials). When examining face matching measures, DPs exhibited a similar distribution of performance as controls, though shifted towards impairment by an average of 1.4 SD. We next applied Bennetts (2022) hierarchical clustering approach and k-means clustering to the CFPT upright, inverted, and inversion index measures, similarly finding one group of DPs with poorer inverted face performance and another with a decreased face inversion effect (holistic processing). However, these subgroup differences failed to generalize to other measures of feature and holistic processing beyond the CFPT. We finally ran hierarchical and k-means cluster analyses on our larger battery of face matching, feature, and holistic processing measures. Results clearly showed subgroups with generally better versus worse performance across all measures, with the distinction between groups being somewhat arbitrary. Together, these findings support a continuous account of DP perceptual heterogeneity, with performance differing primarily across all aspects of face perception.

Neural computations in prosopagnosia.

We report an investigation of the neural processes involved in the processing of faces and objects of brain-lesioned patient PS, a well-documented case of pure acquired prosopagnosia. We gathered a substantial dataset of high-density electrophysiological recordings from both PS and neurotypicals. Using representational similarity analysis, we produced time-resolved brain representations in a format that facilitates direct comparisons across time points, different individuals, and computational models. To understand how the lesions in PS's ventral stream affect the temporal evolution of her brain representations, we computed the temporal generalization of her brain representations. We uncovered that PS's early brain representations exhibit an unusual similarity to later representations, implying an excessive generalization of early visual patterns. To reveal the underlying computational deficits, we correlated PS' brain representations with those of deep neural networks (DNN). We found that the computations underlying PS' brain activity bore a closer resemblance to early layers of a visual DNN than those of controls. However, the brain representations in neurotypicals became more akin to those of the later layers of the model compared to PS. We confirmed PS's deficits in high-level brain representations by demonstrating that her brain representations exhibited less similarity with those of a DNN of semantics.

Human genetics of face recognition: discovery of MCTP2 mutations in humans with face blindness (congenital prosopagnosia).

Face recognition is important for both visual and social cognition. While prosopagnosia or face blindness has been known for seven decades and face-specific neurons for half a century, the molecular genetic mechanism is not clear. Here we report results after 17 years of research with classic genetics and modern genomics. From a large family with 18 congenital prosopagnosia (CP) members with obvious difficulties in face recognition in daily life, we uncovered a fully cosegregating private mutation in the MCTP2 gene which encodes a calcium binding transmembrane protein expressed in the brain. After screening through cohorts of 6589, we found more CPs and their families, allowing detection of more CP associated mutations in MCTP2. Face recognition differences were detected between 14 carriers with the frameshift mutation S80fs in MCTP2 and 19 noncarrying volunteers. Six families including one with 10 members showed the S80fs-CP correlation. Functional magnetic resonance imaging found association of impaired recognition of individual faces by MCTP2 mutant CPs with reduced repetition suppression to repeated facial identities in the right fusiform face area. Our results have revealed genetic predisposition of MCTP2 mutations in CP, 76 years after the initial report of prosopagnosia and 47 years after the report of the first CP. This is the first time a gene required for a higher form of visual social cognition was found in humans.

The neuropsychological evaluation of face identity recognition.

Facial identity recognition (FIR) is arguably the ultimate form of recognition for the adult human brain. Even if the term prosopagnosia is reserved for exceptionally rare brain-damaged cases with a category-specific abrupt loss of FIR at adulthood, subjective and objective impairments or difficulties of FIR are common in the neuropsychological population. Here we provide a critical overview of the evaluation of FIR both for clinicians and researchers in neuropsychology. FIR impairments occur following many causes that should be identified objectively by both general and specific, behavioral and neural examinations. We refute the commonly used dissociation between perceptual and memory deficits/tests for FIR, since even a task involving the discrimination of unfamiliar face images presented side-by-side relies on cortical memories of faces in the right-lateralized ventral occipito-temporal cortex. Another frequently encountered confusion is between specific deficits of the FIR function and a more general impairment of semantic memory (of people), the latter being most often encountered following anterior temporal lobe damage. Many computerized tests aimed at evaluating FIR have appeared over the last two decades, as reviewed here. However, despite undeniable strengths, they often suffer from ecological limitations, difficulties of instruction, as well as a lack of consideration for processing speed and qualitative information. Taking into account these issues, a recently developed behavioral test with natural images manipulating face familiarity, stimulus inversion, and correct response times as a key variable appears promising. The measurement of electroencephalographic (EEG) activity in the frequency domain from fast periodic visual stimulation also appears as a particularly promising tool to complete and enhance the neuropsychological assessment of FIR.

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.

What is developmental about developmental prosopagnosia?

Developmental prosopagnosia (DP) is characterised by difficulties recognising face identities and is associated with diverse co-occurring object recognition difficulties. The high co-occurrence rate and heterogeneity of associated difficulties in DP is an intrinsic feature of developmental conditions, where co-occurrence of difficulties is the rule, rather than the exception. However, despite its name, cognitive and neural theories of DP rarely consider the developmental context in which these difficulties occur. This leaves a large gap in our understanding of how DP emerges in light of the developmental trajectory of face recognition. Here, we argue that progress in the field requires re-considering the developmental origins of differences in face recognition abilities, rather than studying the end-state alone. In practice, considering development in DP necessitates a re-evaluation of current approaches in recruitment, design, and analyses.

Both identity and non-identity face perception tasks predict developmental prosopagnosia and face recognition ability.

Developmental prosopagnosia (DP) is characterised by deficits in face identification. However, there is debate about whether these deficits are primarily perceptual, and whether they extend to other face processing tasks (e.g., identifying emotion, age, and gender; detecting faces in scenes). In this study, 30 participants with DP and 75 controls completed a battery of eight tasks assessing four domains of face perception (identity; emotion; age and gender; face detection). The DP group performed worse than the control group on both identity perception tasks, and one task from each other domain. Both identity perception tests uniquely predicted DP/control group membership, and performance on two measures of face memory. These findings suggest that deficits in DP may arise from issues with face perception. Some non-identity tasks also predicted DP/control group membership and face memory, even when face identity perception was accounted for. Gender perception and speed of face detection consistently predicted unique variance in group membership and face memory; several other tasks were only associated with some measures of face recognition ability. These findings indicate that face perception deficits in DP may extend beyond identity perception. However, the associations between tasks may also reflect subtle aspects of task demands or stimuli.

Relationship between face recognition ability and anxiety tendencies in healthy young individuals: A prosopagnosia index and state-trait anxiety inventory study.

Developmental prosopagnosia (DP) is a condition that indicates the inability to recognize individuals by their faces from birth, without any history of brain damage. The assessment of face recognition ability and diagnosis of DP involve the use of face tests such as the Cambridge Face Memory Test (CFMT) and the Cambridge Face Perception Test, along with self-reported measures like the 20-Item Prosopagnosia Index (PI20). Face recognition accuracy is affected by anxiety. However, previous studies on the relationship between face recognition ability and anxiety have not used the PI20 measure. This study aimed to investigate the relationship between self-reported measures of face recognition ability and anxiety tendencies among healthy young individuals for DP diagnosis and its implications. We used a face recognition test, involving the PI20, CFMT, Visual Perception Test for Agnosia-Famous Face Test (VPTA-FFT), and State-Trait Anxiety Inventory (STAI). We assessed the performance of 116 Japanese young adults (75 females, median age of 20.7 years, with a standard deviation of 1.2). Subsequently, we conducted a statistical analysis to examine the relationship between the outcomes of the face recognition tests and STAI scores using Pearson correlation analysis and single correlation coefficients. The results showed a positive correlation between state anxiety and PI20 (r = 0.308, p = 0.007), and a weak positive correlation was also observed between trait anxiety and PI20 (r = 0.268, p = 0.04). In contrast, there was no correlation between CFMT and VPTA-FFT with respect to STAI. The results of the hierarchical multiple regression analysis also suggested that the correlation between the performance on the PI20 (self-report) and objective measures of face recognition performance (the CFMT and the VPTA-FFT) are driven by differences in anxiety. This study is the first to explore the relationship between face recognition abilities and anxiety using the PI20 self-report measure. There are implications for future research on the diagnosis of DP and the relationship between anxiety and face recognition.

A new way of classifying developmental prosopagnosia: Balanced Integration Score.

Despite severe everyday problems recognising faces, some individuals with developmental prosopagnosia (DP) can achieve typical accuracy scores on laboratory face recognition tests. To address this, studies sometimes also examine response times (RTs), which tend to be longer in DPs relative to control participants. In the present study, 24 potential (according to self-report) DPs and 110 age-matched controls completed the Cambridge Face and Bicycle Memory Tests, old new faces task, and a famous faces test. We used accuracy and the Balanced Integration Score (BIS), a measure that adjusts accuracy for RTs, to classify our sample at the group and individual levels. Subjective face recognition ability was assessed using the PI20 questionnaire and semi structured interviews. Fifteen DPs showed a major impairment using BIS compared with only five using accuracy alone. Logistic regression showed that a model incorporating the BIS measures was the most sensitive for classifying DP and showed highest area under the curve (AUC). Furthermore, larger between-group effect sizes were observed for a derived global (averaged) memory measure calculated using BIS versus accuracy alone. BIS is thus an extremely sensitive novel measure for attenuating speed-accuracy trade-offs that can otherwise mask impairment measured only by accuracy in DP.

The anterior fusiform gyrus: The ghost in the cortical face machine.

Face-selective regions in the human ventral occipito-temporal cortex (VOTC) have been defined for decades mainly with functional magnetic resonance imaging. This face-selective VOTC network is traditionally divided in a posterior 'core' system thought to subtend face perception, and regions of the anterior temporal lobe as a semantic memory component of an extended general system. In between these two putative systems lies the anterior fusiform gyrus and surrounding sulci, affected by magnetic susceptibility artifacts. Here we suggest that this methodological gap overlaps with and contributes to a conceptual gap between (visual) perception and semantic memory for faces. Filling this gap with intracerebral recordings and direct electrical stimulation reveals robust face-selectivity in the anterior fusiform gyrus and a crucial role of this region, especially in the right hemisphere, in identity recognition for both familiar and unfamiliar faces. Based on these observations, we propose an integrated theoretical framework for human face (identity) recognition according to which face-selective regions in the anterior fusiform gyrus join the dots between posterior and anterior cortical face memories.

Intracerebral electrical stimulation of the face-selective right lateral fusiform gyrus transiently impairs face identity recognition.

Neuroimaging and intracranial electrophysiological studies have consistently shown the largest and most consistent face-selective neural activity in the middle portion of the human right lateral fusiform gyrus ('fusiform face area(s)', FFA). Yet, direct evidence for the critical role of this region in face identity recognition (FIR) is still lacking. Here we report the first evidence of transient behavioral impairment of FIR during focal electrical stimulation of the right FFA. Upon stimulation of an electrode contact within this region, subject CJ, who shows typical FIR ability outside of stimulation, was transiently unable to point to pictures of famous faces among strangers and to match pictures of famous or unfamiliar faces presented simultaneously for their identity. Her performance at comparable tasks with other visual materials (written names, pictures of buildings) remained unaffected by stimulation at the same location. During right FFA stimulation, CJ consistently reported that simultaneously presented faces appeared as being the same identity, with little or no distortion of the spatial face configuration. Independent electrophysiological recordings showed the largest neural face-selective and face identity activity at the critical electrode contacts. Altogether, this extensive multimodal case report supports the causal role of the right FFA in FIR.

Provoked overt recognition in acquired prosopagnosia using multiple different images of famous faces.

Provoked overt recognition refers to the fact that patients with acquired prosopagnosia can sometimes recognize faces when presented in arrays of individuals from the same category (e.g., actors or politicians). We ask whether a prosopagnosic patient might experience recognition when presented with multiple different images of the same face simultaneously. Over two sessions, patient Herschel, a 66-year-old British man with acquired prosopagnosia, viewed face images individually or in arrays. On several occasions he failed to recognize single photos of an individual but successfully identified that person when the same photos were presented together. For example, Herschel failed to recognize any individual images of King Charles or Paul McCartney but recognised both in arrays of the same photos. Like reports based on category membership, overt recognition was transient and inconsistent. These findings are discussed in terms of models of covert recognition, alongside more recent research on within-person variability for face perception.

Are people with autism prosopagnosic?

Difficulties in various face processing tasks have been well documented in autism spectrum disorder (ASD). Several meta-analyses and numerous case-control studies have indicated that this population experiences a moderate degree of impairment, with a small percentage of studies failing to detect any impairment. One possible account of this mixed pattern of findings is heterogeneity in face processing abilities stemming from the presence of a subpopulation of prosopagnosic individuals with ASD alongside those with normal face processing skills. Samples randomly drawn from such a population, especially relatively smaller ones, would vary in the proportion of participants with prosopagnosia, resulting in a wide range of group-level deficits from mild (or none) to severe across studies. We test this prosopagnosic subpopulation hypothesis by examining three groups of participants: adults with ASD, adults with developmental prosopagnosia (DP), and a comparison group. Our results show that the prosopagnosic subpopulation hypothesis does not account for the face impairments in the broader autism spectrum. ASD observers show a continuous and graded, rather than categorical, heterogeneity that span a range of face processing skills including many with mild to moderate deficits, inconsistent with a prosopagnosic subtype account. We suggest that pathogenic origins of face deficits for at least some with ASD differ from those of DP.

The role of visual imagery in face recognition and the construction of facial composites. Evidence from Aphantasia.

People with aphantasia have a markedly impaired ability to form visual images in the mind's eye. Here, by testing people with and without aphantasia, we examine the relationship between visual imagery and face processing. We show that aphantasics have weaker face recognition than people with visual imagery, using both self-report (Prosopagnosia Index) and behavioural measures (Cambridge Face Memory Test). However, aphantasics nonetheless have a fully intact ability to construct facial composites from memory (i.e., composites produced using EFIT6 by aphantasics and imagers were rated as equally accurate in terms of their resemblance to a target face). Additionally, we show that aphantasics were less able than imagers to see the resemblance between composites and a target face, suggestive of potential issues with face matching (perception). Finally, we show that holistic and featural methods of composite construction using EFIT6 produce equally accurate composites. Our results suggest that face recognition, but not face composite construction, is facilitated by the ability to represent visual properties as 'pictures in the mind'. Our findings have implications for the study of aphantasia, and also for forensic settings, where face composite systems are commonly used to aid criminal investigations.

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.

Why can people with developmental prosopagnosia recognise some familiar faces? Insights from subjective experience.

Developmental prosopagnosia is a relatively common visuo-cognitive condition, characterised by impaired facial identity recognition. Impairment severity appears to reside on a continuum, however, it is unknown whether instances of milder deficits reflect the successful use of spontaneous (typical) face recognition strategies, or the application of extraneous compensatory cues to recognition. Here, we explore this issue in two studies. First, 23 adults with developmental prosopagnosia were asked about their use of spontaneous versus compensatory face recognition techniques in everyday life, using a series of closed- and open-ended questions. Second, the same participants performed a computerised famous face recognition task where they were asked to provide reasons why they could make any successful identifications. Findings from both studies suggest that people with developmental prosopagnosia can successfully, and quite frequently, use compensatory strategies to recognition, and that these cues support the majority of instances of preserved familiar face recognition. In contrast, 16 of the 23 participants were able to spontaneously recognise familiar faces on at least some occasions, but there were vast individual differences in frequencies of success. These findings have important implications for our conceptualisation of the condition, as well as for diagnostic practice.

No increased prevalence of prosopagnosia in aphantasia: Visual recognition deficits are small and not restricted to faces.

Aphantasia and prosopagnosia are both rare conditions with impairments in visual cognition. While prosopagnosia refers to a face recognition deficit, aphantasics exhibit a lack of mental imagery. Current object recognition theories propose an interplay of perception and mental representations, making an association between recognition performance and visual imagery plausible. While the literature assumes a link between aphantasia and prosopagnosia, other impairments in aphantasia have been shown to be rather global. Therefore, we assumed that aphantasics do not solely exhibit impairments in face recognition but rather in general visual recognition performance, probably moderated by stimulus complexity. To test this hypothesis, 65 aphantasics were compared to 55 controls in a face recognition task, the Cambridge Face Memory Test, and a corresponding object recognition task, the Cambridge Car Memory Test. In both tasks, aphantasics performed worse than controls, indicating mild recognition deficits without face-specificity. Additional correlations between imagery vividness and performance in both tasks were found, suggesting that visual imagery influences visual recognition not only in imagery extremes. Stimulus complexity produced the expected moderation effect but only for the whole imagery-spectrum and only with face stimuli. Overall, the results imply that aphantasia is linked to a general but mild deficit in visual recognition.

Recognition of animal faces is impaired in developmental prosopagnosia.

An on-going debate in psychology and neuroscience concerns the way faces and objects are represented. Domain-specific theories suggest that faces are processed via a specialised mechanism, separate from objects. Developmental prosopagnosia (DP) is a neurodevelopmental disorder in which there is a deficit in the ability to recognize conspecific (human) faces. It is unclear, however, whether prosopagnosia also affects recognition of heterospecific (animal) faces. To address this question, we compared recognition performance with human and animal faces in neurotypical controls and participants with DP. We found that DPs showed deficits in the recognition of both human and animal faces compared to neurotypical controls. In contrast to, we found no group-level deficit in the recognition of animate or inanimate non-face objects in DPs. Using an individual-level approach, we demonstrate that in 60% of cases in which face recognition is impaired, there is a concurrent deficit with animal faces. Together, these results show that DPs have a general deficit in the recognition of faces that encompass a range of configural and morphological structures.

Dissociations between face identity and face expression processing in developmental prosopagnosia.

Individuals with developmental prosopagnosia (DPs) experience severe and lifelong deficits recognising faces, but whether their deficits are selective to the processing of face identity or extend to the processing of face expression remains unclear. Clarifying this issue is important for understanding DP impairments and advancing theories of face processing. We compared identity and expression processing in a large sample of DPs (N = 124) using three different matching tasks that each assessed identity and expression processing with identical experimental formats. We ran each task in upright and inverted orientations and we measured inversion effects to assess the integrity of upright-specific face processes. We report three main results. First, DPs showed large deficits at discriminating identity but only subtle deficits at discriminating expression. Second, DPs showed a reduced inversion effect for identity but a normal inversion effect for expression. Third, DPs' performance on the expression tasks were linked to autism traits, but their performance on the identity tasks were not. These results constitute several dissociations between identity and expression processing in DP, and they are consistent with the view that the core impairment in DP is highly selective to identity.