Face Feature Change Detection Ability in Developmental Prosopagnosia and Super-Recognisers.

In non-clinical populations, facial features (eyes, nose, mouth) may vary in their contribution to face identity perception. Changes to whole faces are easier to detect than changes to individual features, and eye changes are typically easier to detect than mouth changes, which in turn are easier to detect than nose changes. However, how this differs for people with face recognition difficulties (developmental prosopagnosia; DP) and for individuals with superior face recognition abilities (super-recognisers; SR) is not clear; although findings from previous studies have suggested differences, the nature of this difference is not understood. The aim of this study was to examine whether differences in the ability to detect feature changes in DPs and SRs were (a) quantitative, meaning that the pattern across feature changes remained the same but there was an overall upwards or downwards shift in performance, or (b) qualitative, meaning that the pattern across feature changes was different. Using a change detection task in which individual face features (eyes, nose, mouth) changed between sequentially presented faces, we found that while prosopagnosics showed a quantitative difference in performance with a downwards shift across all conditions, super-recognisers only showed qualitative differences: they were better able to detect when the face was the same and were marginally (but not non-significantly) worse at detecting when the eyes changed. Further, the only condition which distinguished between the three groups was the ability to identify when the same face was presented, with SRs being better than controls, and controls being better than DPs. Our findings suggest that, in feature-matching tasks, differences for DPs are due to them being overall worse at the task, while SRs use a qualitatively different strategy.

Neural responses in a fast periodic visual stimulation paradigm reveal domain-general visual discrimination deficits in developmental prosopagnosia.

We investigated selective impairments of visual identity discrimination in developmental prosopagnosia (DP), using a fast periodic identity oddball stimulation paradigm with electroencephalography (EEG). In Experiment 1, neural responses to unfamiliar face identity changes were strongly attenuated for individuals with DP as compared to Control participants, to the same extent for upright and inverted faces. This reduction of face identity discrimination responses, which was confirmed in Experiment 2, provides direct evidence for deficits in the visual processing of unfamiliar facial identity in DP. Importantly, Experiment 2 demonstrated that DPs showed attenuated neural responses to identity oddballs not only with face images, but also with non-face images (cars). This result strongly suggests that rapid identity-related visual processing impairments in DP are not restricted to faces, but also affect familiar classes of non-face stimuli. Visual discrimination deficits in DP do not appear to be face-specific. To account for these findings, we propose a new account of DP as a domain-general deficit in rapid visual discrimination.

Holistic face perception is impaired in developmental prosopagnosia.

Individuals with developmental prosopagnosia (DP) have severe difficulties recognising familiar faces. A current debate is whether these face recognition impairments derive from problems with face perception and in particular whether individuals with DP cannot utilize holistic representations of individual faces. To assess this hypothesis, we recorded event-related potentials (ERPs) during a sequential face identity matching task where successively presented pairs of upright faces were either identical or differed with respect to their internal features, their external features, or both. Participants with DP and age-matched controls reported on each trial whether the face pair was identical or different. To track the activation of cortical visual face memory representations, we measured N250r components over posterior face-selective regions. N250r components to full face repetitions were strongly attenuated for DPs as compared to control participants, indicating impaired face identity matching processes in DP. In the Control group, the N250r to full face repetitions was superadditive (i.e., larger than the sum of the two N250r components to partial repetitions of external or internal features). This demonstrates that holistic face representations were involved in identity matching processes. In the DP group, N250r components to full and partial identity repetitions were strictly additive, indicating that the identity matching of external and internal features operated in an entirely part-based fashion, without any involvement of holistic representations. In line with this conclusion, DPs also made a disproportionate number of errors on partial repetition trials, where they often failed to report a change of internal facial features. This suggests an atypical strategy for encoding external features as cues to identity in DP. These results provide direct electrophysiological and behavioural evidence for qualitative differences in the representation of face identity in the occipital-temporal face processing system in developmental prosopagnosia.

Face identity matching is selectively impaired in developmental prosopagnosia.

Individuals with developmental prosopagnosia (DP) have severe face recognition deficits, but the mechanisms that are responsible for these deficits have not yet been fully identified. We assessed whether the activation of visual working memory for individual faces is selectively impaired in DP. Twelve DPs and twelve age-matched control participants were tested in a task where they reported whether successively presented faces showed the same or two different individuals, and another task where they judged whether the faces showed the same or different facial expressions. Repetitions versus changes of the other currently irrelevant attribute were varied independently. DPs showed impaired performance in the identity task, but performed at the same level as controls in the expression task. An electrophysiological marker for the activation of visual face memory by identity matches (N250r component) was strongly attenuated in the DP group, and the size of this attenuation was correlated with poor performance in a standardized face recognition test. Results demonstrate an identity-specific deficit of visual face memory in DPs. Their reduced sensitivity to identity matches in the presence of other image changes could result from earlier deficits in the perceptual extraction of image-invariant visual identity cues from face images.

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.

Electrophysiological evidence for parts and wholes in visual face memory.

It is often assumed that upright faces are represented in a holistic fashion, while representations of inverted faces are essentially part-based. To assess this hypothesis, we recorded event-related potentials (ERPs) during a sequential face identity matching task where successively presented pairs of upright or inverted faces were either identical or differed with respect to their internal features, their external features, or both. Participants' task was to report on each trial whether the face pair was identical or different. To track the activation of visual face memory representations, we measured N250r components that emerge over posterior face-selective regions during the activation of visual face memory representations by a successful identity match. N250r components to full identity repetitions were smaller and emerged later for inverted as compared to upright faces, demonstrating that image inversion impairs face identity matching processes. For upright faces, N250r components were also elicited by partial repetitions of external or internal features, which suggest that the underlying identity matching processes are not exclusively based on non-decomposable holistic representations. However, the N250r to full identity repetitions was super-additive (i.e., larger than the sum of the two N250r components to partial repetitions of external or internal features) for upright faces, demonstrating that holistic representations were involved in identity matching processes. For inverted faces, N250r components to full and partial identity repetitions were strictly additive, indicating that the identity matching of external and internal features operated in an entirely part-based fashion. These results provide new electrophysiological evidence for qualitative differences between representations of upright and inverted faces in the occipital-temporal face processing system.

Reduced sensitivity to contrast signals from the eye region in developmental prosopagnosia.

Contrast-related signals from the eye region are known to be important for the processing of facial identity. Individuals with developmental prosopagnosia (DP) have severe face recognition problems, which may be linked to deficits in the perceptual processing of identity-related information from the eyes. We tested this hypothesis by measuring N170 components in DP participants and age-matched controls in response to face images where the contrast polarity of the eyes and of other face parts was independently manipulated. In different trials, participants fixated either the eye region or the lower part of a face. In the Control group, contrast-reversal of the eyes resulted in enhanced and delayed N170 components, irrespective of the contrast of other face parts and of gaze location. In the DP group, these effects of eye contrast on N170 amplitudes were strongly and significantly reduced, demonstrating that perceptual face processing in DP is less well tuned to contrast information from the eye region. Inverting the contrast of other parts of the face affected N170 amplitudes only when fixation was outside the eye region. This effect did not differ between the two groups, indicating that DPs are not generally insensitive to the contrast polarity of face images. These results provide new evidence that a selective deficit in detecting and analysing identity-related information provided by contrast signals from the eye region may contribute to the face recognition impairment in DP.

Facial identity and facial expression are initially integrated at visual perceptual stages of face processing.

It is frequently assumed that facial identity and facial expression are analysed in functionally and anatomically distinct streams within the core visual face processing system. To investigate whether expression and identity interact during the visual processing of faces, we employed a sequential matching procedure where participants compared either the identity or the expression of two successively presented faces, and ignored the other irrelevant dimension. Repetitions versus changes of facial identity and expression were varied independently across trials, and event-related potentials (ERPs) were recorded during task performance. Irrelevant facial identity and irrelevant expression both interfered with performance in the expression and identity matching tasks. These symmetrical interference effects show that neither identity nor expression can be selectively ignored during face matching, and suggest that they are not processed independently. N250r components to identity repetitions that reflect identity matching mechanisms in face-selective visual cortex were delayed and attenuated when there was an expression change, demonstrating that facial expression interferes with visual identity matching. These findings provide new evidence for interactions between facial identity and expression within the core visual processing system, and question the hypothesis that these two attributes are processed independently.

Normal perception of Mooney faces in developmental prosopagnosia: Evidence from the N170 component and rapid neural adaptation.

Individuals with developmental prosopagnosia (DP) have a severe difficulty recognizing the faces of known individuals in the absence of any history of neurological damage. These recognition problems may be linked to selective deficits in the holistic/configural processing of faces. We used two-tone Mooney images to study the processing of faces versus non-face objects in DP when it is based on holistic information (or the facial gestalt) in the absence of obvious local cues about facial features. A rapid adaptation procedure was employed for a group of 16 DPs. Naturalistic photographs of upright faces were preceded by upright or inverted Mooney faces or by Mooney houses. DPs showed face-sensitive N170 components in response to Mooney faces versus houses, and N170 amplitude reductions for inverted as compared to upright Mooney faces. They also showed the typical pattern of N170 adaptation effects, with reduced N170 components when upright naturalistic test faces were preceded by upright Mooney faces, demonstrating that the perception of Mooney and naturalistic faces recruits shared neural populations. Our findings demonstrate that individuals with DP can utilize global information about face configurations for categorical discriminations between faces and non-face objects, and suggest that face processing deficits emerge primarily at more fine-grained higher level stages of face perception.

Perceptual face processing in developmental prosopagnosia is not sensitive to the canonical location of face parts.

Individuals with developmental prosopagnosia (DP) are strongly impaired in recognizing faces, but it is controversial whether this deficit is linked to atypical visual-perceptual face processing mechanisms. Previous behavioural studies have suggested that face perception in DP might be less sensitive to the canonical spatial configuration of face parts in upright faces. To test this prediction, we recorded event-related brain potentials (ERPs) to intact upright faces and to faces with spatially scrambled parts (eyes, nose, and mouth) in a group of ten participants with DP and a group of ten age-matched control participants with normal face recognition abilities. The face-sensitive N170 component and the vertex positive potential (VPP) were both enhanced and delayed for scrambled as compared to intact faces in the control group. In contrast, N170 and VPP amplitude enhancements to scrambled faces were absent in the DP group. For control participants, the N170 to scrambled faces was also sensitive to feature locations, with larger and delayed N170 components contralateral to the side where all features appeared in a non-canonical position. No such differences were present in the DP group. These findings suggest that spatial templates of the prototypical feature locations within an upright face are selectively impaired in DP.

The Focus of Spatial Attention Determines the Number and Precision of Face Representations in Working Memory.

The capacity of visual working memory for faces is extremely limited, but the reasons for these limitations remain unknown. We employed event-related brain potential measures to demonstrate that individual faces have to be focally attended in order to be maintained in working memory, and that attention is allocated to only a single face at a time. When 2 faces have to be memorized simultaneously in a face identity-matching task, the focus of spatial attention during encoding predicts which of these faces can be successfully maintained in working memory and matched to a subsequent test face. We also show that memory representations of attended faces are maintained in a position-dependent fashion. These findings demonstrate that the limited capacity of face memory is directly linked to capacity limits of spatial attention during the encoding and maintenance of individual face representations. We suggest that the capacity and distribution of selective spatial attention is a dynamic resource that constrains the capacity and fidelity of working memory for faces.

Effects of contrast inversion on face perception depend on gaze location: Evidence from the N170 component.

Face recognition is known to be impaired when the contrast polarity of the eyes is inverted. We studied how contrast affects early perceptual face processing by measuring the face-sensitive N170 component to face images when the contrast of the eyes and of the rest of the face was independently manipulated. Fixation was either located on the eye region or on the lower part of a face. Contrast-reversal of the eyes triggered delayed and enhanced N170 components independently of the contrast of other face parts, and regardless of gaze location. Similar N170 modulations were observed when the rest of a face was contrast-inverted, but only when gaze was directed away from the eyes. Results demonstrate that the contrast of the eyes and of other face parts can both affect face perception, but that the contrast polarity of the eye region has a privileged role during early stages of face processing.

Facial misidentifications arise from the erroneous activation of visual face memory.

Misidentifications are a common phenomenon in unfamiliar face processing, but little is known about the underlying cognitive and neural mechanisms. We used the face identity-sensitive N250r component of the event-related brain potential as a measure of identity-sensitive face matching process in visual working memory. Two face images were presented in rapid succession, and participants had to judge whether they showed the same or two different individuals. Identity match and mismatch trials were presented in random sequence. On similar mismatch trials, perceptually similar faces of two different individuals were shown, while two physically distinct faces were presented on dissimilar mismatch trials. Misidentification errors occurred on 40% of all similar mismatch trials. N250r components were elicited not only in response to an identity match, but also on trials with misidentification errors. This misidentification N250r was smaller and emerged later than the N250r to correctly detected identity repetitions. Importantly, N250r components were entirely eliminated on similar mismatch trials where participants correctly reported two different facial identities. Results show that misidentification errors are not primarily a post-perceptual decision-related phenomenon, but are generated during early visual stages of identity-related face processing. Misidentification errors occur when stored representations of a particular individual face in visual working memory are incorrectly activated by a perceptual match with a different face.

The activation of visual face memory and explicit face recognition are delayed in developmental prosopagnosia.

Individuals with developmental prosopagnosia (DP) are strongly impaired in recognizing faces, but the causes of this deficit are not well understood. We employed event-related brain potentials (ERPs) to study the time-course of neural processes involved in the recognition of previously unfamiliar faces in DPs and in age-matched control participants with normal face recognition abilities. Faces of different individuals were presented sequentially in one of three possible views, and participants had to detect a specific Target Face ("Joe"). EEG was recorded during task performance to Target Faces, Nontarget Faces, or the participants' Own Face (which had to be ignored). The N250 component was measured as a marker of the match between a seen face and a stored representation in visual face memory. The subsequent P600f was measured as an index of attentional processes associated with the conscious awareness and recognition of a particular face. Target Faces elicited reliable N250 and P600f in the DP group, but both of these components emerged later in DPs than in control participants. This shows that the activation of visual face memory for previously unknown learned faces and the subsequent attentional processing and conscious recognition of these faces are delayed in DP. N250 and P600f components to Own Faces did not differ between the two groups, indicating that the processing of long-term familiar faces is less affected in DP. However, P600f components to Own Faces were absent in two participants with DP who failed to recognize their Own Face during the experiment. These results provide new evidence that face recognition deficits in DP may be linked to a delayed activation of visual face memory and explicit identity recognition mechanisms.

Early stages of perceptual face processing are confined to the contralateral hemisphere: evidence from the N170 component.

High-level visual object processing is often assumed to be largely position-independent. Here we demonstrate that when faces and non-face objects simultaneously appear in opposite visual hemifields, the face-sensitive N170 component of the event-related brain potential (ERP) is exclusively generated in the contralateral hemisphere. The effects of face inversion on N170 amplitudes and latencies also show strong contralateral biases. These results reveal that retinotopic biases in low-level visual cortex extend well into category-selective high-level vision. We suggest that the contralateral organisation of face-sensitive visual processing results from generic competitive interactions between hemispheres during the simultaneous perception of visual objects.

Social inferences from faces: ambient images generate a three-dimensional model.

Three experiments are presented that investigate the two-dimensional valence/trustworthiness by dominance model of social inferences from faces (Oosterhof & Todorov, 2008). Experiment 1 used image averaging and morphing techniques to demonstrate that consistent facial cues subserve a range of social inferences, even in a highly variable sample of 1000 ambient images (images that are intended to be representative of those encountered in everyday life, see Jenkins, White, Van Montfort, & Burton, 2011). Experiment 2 then tested Oosterhof and Todorov's two-dimensional model on this extensive sample of face images. The original two dimensions were replicated and a novel 'youthful-attractiveness' factor also emerged. Experiment 3 successfully cross-validated the three-dimensional model using face averages directly constructed from the factor scores. These findings highlight the utility of the original trustworthiness and dominance dimensions, but also underscore the need to utilise varied face stimuli: with a more realistically diverse set of face images, social inferences from faces show a more elaborate underlying structure than hitherto suggested.

The face-sensitive N170 component in developmental prosopagnosia.

Individuals with developmental prosopagnosia (DP) show severe face recognition deficits in the absence of any history of neurological damage. To examine the time-course of face processing in DP, we measured the face-sensitive N170 component of the event-related brain potential (ERP) in a group of 16 participants with DP and 16 age-matched control participants. Reliable enhancements of N170 amplitudes in response to upright faces relative to houses were found for the DP group. This effect was equivalent in size to the effect observed for controls, demonstrating normal face-sensitivity of the N170 component in DP. Face inversion enhanced N170 amplitudes in the control group, but not for DPs, suggesting that many DPs do not differentiate between upright and inverted faces in the typical manner. These N170 face inversion effects were present for younger but not older controls, while they were absent for both younger and older DPs. Results suggest that the early face-sensitivity of visual processing is preserved in most individuals with DP, but that the face processing system in many DPs is not selectively tuned to the canonical upright orientation of faces.

Electrophysiological studies of face processing in developmental prosopagnosia: neuropsychological and neurodevelopmental perspectives.

People with developmental prosopagnosia (DP) show severe face-recognition deficits that typically emerge during childhood without history of neurological damage. We review findings from recent event-related brain potential (ERP) studies of face perception and face recognition in DP. The generic face-sensitivity of the N170 component is present in most DPs, suggesting rapid category-selective streaming of facial information. In contrast, DPs show atypical N170 face inversion effects, indicative of impaired structural encoding, specifically for upright faces. In line with neurodevelopmental accounts of DP, these effects are similar to those observed for other developmental disorders, as well as for younger children and older adults. Identity-sensitive ERP components (N250, P600f) triggered during successful face recognition are similar for DPs and control participants, indicating that the same mechanisms are active in both groups. The presence of covert face-recognition effects for the N250 component suggests that visual face memory and semantic memory can become disconnected in some individuals with DP. The implications of these results for neuropsychological and neurodevelopmental perspectives on DP are discussed.

Response of face-selective brain regions to trustworthiness and gender of faces.

Neuropsychological and neuroimaging studies have demonstrated a role for the amygdala in processing the perceived trustworthiness of faces, but it remains uncertain whether its responses are linear (with the greatest response to the least trustworthy-looking faces), or quadratic (with increased fMRI signal for the dimension extremes). It is also unclear whether the trustworthiness of the stimuli is crucial or if the same response pattern can be found for faces varying along other dimensions. In addition, the responses to perceived trustworthiness of face-selective regions other than the amygdala are seldom reported. The present study addressed these issues using a novel set of stimuli created through computer image-manipulation both to maximise the presence of naturally occurring cues that underpin trustworthiness judgments and to allow systematic manipulation of these cues. With a block-design fMRI paradigm, we investigated neural responses to computer-manipulated trustworthiness in the amygdala and core face-selective regions in the occipital and temporal lobes. We asked whether the activation pattern is specific for differences in trustworthiness or whether it would also track variation along an orthogonal male-female gender dimension. The main findings were quadratic responses to changes in both trustworthiness and gender in all regions. These results are consistent with the idea that face-responsive brain regions are sensitive to face distinctiveness as well as the social meaning of the face features.