Face perception across the adult lifespan: evidence for age-related changes independent of general intelligence.

It is well-documented that face perception - including facial expression and identity recognition ability - declines with age. To date, however, it is not yet well understood whether this age-related decline reflects face-specific effects, or instead can be accounted for by well-known declines in general intelligence. We examined this issue using a relatively large, healthy, age-diverse (18-88 years) sample (N = 595) who were assessed on well-established measures of face perception and general intelligence. Replicating previous work, we observed that facial expression recognition, facial identity recognition, and general intelligence all showed declines with age. Of importance, the age-related decline of expression and identity recognition was present even when the effects of general intelligence were statistically controlled. Moreover, facial expression and identity ability each showed significant unique associations with age. These results indicate that face perception ability becomes poorer as we age, and that this decline is to some extent relatively focal in nature. Results are in line with a hierarchical structure of face perception ability, and suggest that age appears to have independent effects on the general and specific face processing levels within this structure.

Symmetrical Viewpoint Representations in Face-Selective Regions Convey an Advantage in the Perception and Recognition of Faces.

Learning new identities is crucial for effective social interaction. A critical aspect of this process is the integration of different images from the same face into a view-invariant representation that can be used for recognition. The representation of symmetrical viewpoints has been proposed to be a key computational step in achieving view-invariance. The aim of this study was to determine whether the representation of symmetrical viewpoints in face-selective regions is directly linked to the perception and recognition of face identity. In Experiment 1, we measured fMRI responses while male and female human participants viewed images of real faces from different viewpoints (-90, -45, 0, 45, and 90° from full-face view). Within the face regions, patterns of neural response to symmetrical views (-45 and 45° or -90 and 90°) were more similar than responses to nonsymmetrical views in the fusiform face area and superior temporal sulcus, but not in the occipital face area. In Experiment 2, participants made perceptual similarity judgements to pairs of face images. Images with symmetrical viewpoints were reported as being more similar than nonsymmetric views. In Experiment 3, we asked whether symmetrical views also convey an advantage when learning new faces. We found that recognition was best when participants were tested with novel face images that were symmetrical to the learning viewpoint. Critically, the pattern of perceptual similarity and recognition across different viewpoints predicted the pattern of neural response in face-selective regions. Together, our results provide support for the functional value of symmetry as an intermediate step in generating view-invariant representations.SIGNIFICANCE STATEMENT The recognition of identity from faces is crucial for successful social interactions. A critical step in this process is the integration of different views into a unified, view-invariant representation. The representation of symmetrical views (e.g., left profile and right profile) has been proposed as an important intermediate step in computing view-invariant representations. We found view symmetric representations were specific to some face-selective regions, but not others. We also show that these neural representations influence the perception of faces. Symmetric views were perceived to be more similar and were recognized more accurately than nonsymmetric views. Moreover, the perception and recognition of faces at different viewpoints predicted patterns of response in those face regions with view symmetric representations.

Prediction-error signals to violated expectations about person identity and head orientation are doubly-dissociated across dorsal and ventral visual stream regions.

Predictive coding theories of perception highlight the importance of constantly updated internal models of the world to predict future sensory inputs. Importantly, such theories suggest that prediction-error signalling should be specific to the violation of predictions concerning distinct attributes of the same stimulus. To interrogate this as yet untested prediction, we focused on two different aspects of face perception (identity and orientation) and investigated whether cortical regions which process particular stimulus attributes also signal prediction violations with respect to those same stimulus attributes. We employed a paradigm using sequential trajectories of images to create perceptual expectations about face orientation and identity, and then parametrically violated each attribute. Using MEG data, we identified double dissociations of expectancy violations in the dorsal and ventral visual streams, such that the right fusiform gyrus showed greater prediction-error signals to identity violations than to orientation violations, whereas the left angular gyrus showed the converse pattern of results. Our results suggest that perceptual prediction-error signalling is directly linked to regions associated with the processing of different stimulus properties.

Dose-dependent modulation of the visually evoked N1/N170 by perceptual surprise: a clear demonstration of prediction-error signalling.

Prediction-error checking processes play a key role in predictive coding models of perception. However, neural indices of such processes have yet to be unambiguously demonstrated. To date, experimental paradigms aiming to study such phenomena have relied upon the relative frequency of stimulus repeats and/or 'unexpected' events that are physically different from 'expected' events. These features of experimental design leave open alternative explanations for the observed effects. A definitive demonstration requires that presumed prediction error-related responses should show contextual dependency (rather than simply effects of frequency or repetition) and should not be attributable to low-level stimulus differences. Most importantly, prediction-error signals should show dose dependency with respect to the degree to which expectations are violated. Here, we exploit a novel experimental paradigm specifically designed to address these issues, using it to interrogate early latency event-related potentials (ERPs) to contextually expected and unexpected visual stimuli. In two electroencephalography (EEG) experiments, we demonstrate that an N1/N170 evoked potential is robustly modulated by unexpected perceptual events ('perceptual surprise') and shows dose-dependent sensitivity with respect to both the influence of prior information and the extent to which expectations are violated. This advances our understanding of perceptual predictions in the visual domain by clearly identifying these evoked potentials as an index of visual surprise.

Facial identity across the lifespan.

We can recognise people that we know across their lifespan. We see family members age, and we can recognise celebrities across long careers. How is this possible, despite the very large facial changes that occur as people get older? Here we analyse the statistical properties of faces as they age, sampling photos of the same people from their 20s to their 70s. Across a number of simulations, we observe that individuals' faces retain some idiosyncratic physical properties across the adult lifespan that can be used to support moderate levels of age-independent recognition. However, we found that models based exclusively on image-similarity only achieved limited success in recognising faces across age. In contrast, more robust recognition was achieved with the introduction of a minimal top-down familiarisation procedure. Such models can incorporate the within-person variability associated with a particular individual to show a surprisingly high level of generalisation, even across the lifespan. The analysis of this variability reveals a powerful statistical tool for understanding recognition, and demonstrates how visual representations may support operations typically thought to require conceptual properties.

Consistent evidence of a link between Alexithymia and general intelligence.

Alexithymia is a personality construct characterised most notably by a difficulty in identifying and expressing feelings. Although the emotional difficulties in alexithymia are well established, to date little work has examined its relationship to broader cognitive abilities, such as general intelligence. Across three independent, healthy adult samples (Ns = 389, 318, & 273), we examined whether alexithymia was associated with general intelligence. In all three samples, we observed a significant negative association between alexithymia and general intelligence. In two of the samples, general intelligence was a significant predictor of alexithymia even when accounting for performance on tests of facial emotion recognition ability and supramodal emotion recognition ability (measured with faces, bodies, and voices). From a theoretical perspective, these results suggest that models of alexithymia need to incorporate a role for more generalised cognitive functioning. From a practical perspective, studies examining links between alexithymia and clinical disorders, many of which have known links to general intelligence, should consider including a measure of general intelligence in order to adjust for this potentially confounding factor.

A Robust Neural Index of High Face Familiarity.

Humans are remarkably accurate at recognizing familiar faces, whereas their ability to recognize, or even match, unfamiliar faces is much poorer. However, previous research has failed to identify neural correlates of this striking behavioral difference. Here, we found a clear difference in brain potentials elicited by highly familiar faces versus unfamiliar faces. This effect starts 200 ms after stimulus onset and reaches its maximum at 400 to 600 ms. This sustained-familiarity effect was substantially larger than previous candidates for a neural familiarity marker and was detected in almost all participants, representing a reliable index of high familiarity. Whereas its scalp distribution was consistent with a generator in the ventral visual pathway, its modulation by repetition and degree of familiarity suggests an integration of affective and visual information.

Recognition of facial expression and identity in part reflects a common ability, independent of general intelligence and visual short-term memory.

Recognising identity and emotion conveyed by the face is important for successful social interactions and has thus been the focus of considerable research. Debate has surrounded the extent to which the mechanisms underpinning face emotion and face identity recognition are distinct or share common processes. Here we use an individual differences approach to address this issue. In a well-powered (N = 605) and age-diverse sample we used structural equation modelling to assess the association between face emotion recognition and face identity recognition ability. We also sought to assess whether this association (if present) reflected visual short-term memory and/or general intelligence (g). We observed a strong positive correlation (r = .52) between face emotion recognition ability and face identity recognition ability. This association was reduced in magnitude but still moderate in size (r = .28) and highly significant when controlling for measures of g and visual short-term memory. These results indicate that face emotion and face identity recognition abilities in part share a common processing mechanism. We suggest that face processing ability involves multiple functional components and that modelling the sources of individual differences can offer an important perspective on the relationship between these components.

Distinct but Overlapping Patterns of Response to Words and Faces in the Fusiform Gyrus.

Converging evidence suggests that the fusiform gyrus is involved in the processing of both faces and words. We used fMRI to investigate the extent to which the representation of words and faces in this region of the brain is based on a common neural representation. In Experiment 1, a univariate analysis revealed regions in the fusiform gyrus that were only selective for faces and other regions that were only selective for words. However, we also found regions that showed both word-selective and face-selective responses, particularly in the left hemisphere. We then used a multivariate analysis to measure the pattern of response to faces and words. Despite the overlap in regional responses, we found distinct patterns of response to both faces and words in the left and right fusiform gyrus. In Experiment 2, fMR adaptation was used to determine whether information about familiar faces and names is integrated in the fusiform gyrus. Distinct regions of the fusiform gyrus showed adaptation to either familiar faces or familiar names. However, there was no adaptation to sequences of faces and names with the same identity. Taken together, these results provide evidence for distinct, but overlapping, neural representations for words and faces in the fusiform gyrus.

Modeling first impressions from highly variable facial images.

First impressions of social traits, such as trustworthiness or dominance, are reliably perceived in faces, and despite their questionable validity they can have considerable real-world consequences. We sought to uncover the information driving such judgments, using an attribute-based approach. Attributes (physical facial features) were objectively measured from feature positions and colors in a database of highly variable "ambient" face photographs, and then used as input for a neural network to model factor dimensions (approachability, youthful-attractiveness, and dominance) thought to underlie social attributions. A linear model based on this approach was able to account for 58% of the variance in raters' impressions of previously unseen faces, and factor-attribute correlations could be used to rank attributes by their importance to each factor. Reversing this process, neural networks were then used to predict facial attributes and corresponding image properties from specific combinations of factor scores. In this way, the factors driving social trait impressions could be visualized as a series of computer-generated cartoon face-like images, depicting how attributes change along each dimension. This study shows that despite enormous variation in ambient images of faces, a substantial proportion of the variance in first impressions can be accounted for through linear changes in objectively defined features.

Spatial properties of objects predict patterns of neural response in the ventral visual pathway.

Neuroimaging studies have revealed topographically organised patterns of response to different objects in the ventral visual pathway. These patterns are thought to be based on the form of the object. However, it is not clear what dimensions of object form are important. Here, we determined the extent to which spatial properties (energy across the image) could explain patterns of response in these regions. We compared patterns of fMRI response to images from different object categories presented at different retinal sizes. Although distinct neural patterns were evident to different object categories, changing the size (and thus the spatial properties) of the images had a significant effect on these patterns. Next, we used a computational approach to determine whether more fine-grained differences in the spatial properties can explain the patterns of neural response to different objects. We found that the spatial properties of the image were able to predict patterns of neural response, even when categorical factors were removed from the analysis. We also found that the effect of spatial properties on the patterns of response varies across the ventral visual pathway. These results show how spatial properties can be an important organising principle in the topography of the ventral visual pathway.

Modelling the perceptual similarity of facial expressions from image statistics and neural responses.

The ability to perceive facial expressions of emotion is essential for effective social communication. We investigated how the perception of facial expression emerges from the image properties that convey this important social signal, and how neural responses in face-selective brain regions might track these properties. To do this, we measured the perceptual similarity between expressions of basic emotions, and investigated how this is reflected in image measures and in the neural response of different face-selective regions. We show that the perceptual similarity of different facial expressions (fear, anger, disgust, sadness, happiness) can be predicted by both surface and feature shape information in the image. Using block design fMRI, we found that the perceptual similarity of expressions could also be predicted from the patterns of neural response in the face-selective posterior superior temporal sulcus (STS), but not in the fusiform face area (FFA). These results show that the perception of facial expression is dependent on the shape and surface properties of the image and on the activity of specific face-selective regions.

Modelling verbal aggression, physical aggression and inappropriate sexual behaviour after acquired brain injury.

Understanding the underpinnings of behavioural disturbances following brain injury is of considerable importance, but little at present is known about the relationships between different types of behavioural disturbances. Here, we take a novel approach to this issue by using confirmatory factor analysis to elucidate the architecture of verbal aggression, physical aggression and inappropriate sexual behaviour using systematic records made across an eight-week observation period for a large sample (n = 301) of individuals with a range of brain injuries. This approach offers a powerful test of the architecture of these behavioural disturbances by testing the fit between observed behaviours and different theoretical models. We chose models that reflected alternative theoretical perspectives based on generalized disinhibition (Model 1), a difference between aggression and inappropriate sexual behaviour (Model 2), or on the idea that verbal aggression, physical aggression and inappropriate sexual behaviour reflect broadly distinct but correlated clinical phenomena (Model 3). Model 3 provided the best fit to the data indicating that these behaviours can be viewed as distinct, but with substantial overlap. These data are important both for developing models concerning the architecture of behaviour as well as for clinical management in individuals with brain injury.

Neural responses to expression and gaze in the posterior superior temporal sulcus interact with facial identity.

Neural models of human face perception propose parallel pathways. One pathway (including posterior superior temporal sulcus, pSTS) is responsible for processing changeable aspects of faces such as gaze and expression, and the other pathway (including the fusiform face area, FFA) is responsible for relatively invariant aspects such as identity. However, to be socially meaningful, changes in expression and gaze must be tracked across an individual face. Our aim was to investigate how this is achieved. Using functional magnetic resonance imaging, we found a region in pSTS that responded more to sequences of faces varying in gaze and expression in which the identity was constant compared with sequences in which the identity varied. To determine whether this preferential response to same identity faces was due to the processing of identity in the pSTS or was a result of interactions between pSTS and other regions thought to code face identity, we measured the functional connectivity between face-selective regions. We found increased functional connectivity between the pSTS and FFA when participants viewed same identity faces compared with different identity faces. Together, these results suggest that distinct neural pathways involved in expression and identity interact to process the changeable features of the face in a socially meaningful way.

Morphing between expressions dissociates continuous from categorical representations of facial expression in the human brain.

Whether the brain represents facial expressions as perceptual continua or as emotion categories remains controversial. Here, we measured the neural response to morphed images to directly address how facial expressions of emotion are represented in the brain. We found that face-selective regions in the posterior superior temporal sulcus and the amygdala responded selectively to changes in facial expression, independent of changes in identity. We then asked whether the responses in these regions reflected categorical or continuous neural representations of facial expression. Participants viewed images from continua generated by morphing between faces posing different expressions such that the expression could be the same, could involve a physical change but convey the same emotion, or could differ by the same physical amount but be perceived as two different emotions. We found that the posterior superior temporal sulcus was equally sensitive to all changes in facial expression, consistent with a continuous representation. In contrast, the amygdala was only sensitive to changes in expression that altered the perceived emotion, demonstrating a more categorical representation. These results offer a resolution to the controversy about how facial expression is processed in the brain by showing that both continuous and categorical representations underlie our ability to extract this important social cue.

Brain regions involved in processing facial identity and expression are differentially selective for surface and edge information.

Although different brain regions are widely considered to be involved in the recognition of facial identity and expression, it remains unclear how these regions process different properties of the visual image. Here, we ask how surface-based reflectance information and edge-based shape cues contribute to the perception and neural representation of facial identity and expression. Contrast-reversal was used to generate images in which normal contrast relationships across the surface of the image were disrupted, but edge information was preserved. In a behavioural experiment, contrast-reversal significantly attenuated judgements of facial identity, but only had a marginal effect on judgements of expression. An fMR-adaptation paradigm was then used to ask how brain regions involved in the processing of identity and expression responded to blocks comprising all normal, all contrast-reversed, or a mixture of normal and contrast-reversed faces. Adaptation in the posterior superior temporal sulcus--a region directly linked with processing facial expression--was relatively unaffected by mixing normal with contrast-reversed faces. In contrast, the response of the fusiform face area--a region linked with processing facial identity--was significantly affected by contrast-reversal. These results offer a new perspective on the reasons underlying the neural segregation of facial identity and expression in which brain regions involved in processing invariant aspects of faces, such as identity, are very sensitive to surface-based cues, whereas regions involved in processing changes in faces, such as expression, are relatively dependent on edge-based cues.

The Thatcher illusion reveals orientation dependence in brain regions involved in processing facial expressions.

Although the processing of facial identity is known to be sensitive to the orientation of the face, it is less clear whether orientation sensitivity extends to the processing of facial expressions. To address this issue, we used functional MRI (fMRI) to measure the neural response to the Thatcher illusion. This illusion involves a local inversion of the eyes and mouth in a smiling face-when the face is upright, the inverted features make it appear grotesque, but when the face is inverted, the inversion is no longer apparent. Using an fMRI-adaptation paradigm, we found a release from adaptation in the superior temporal sulcus-a region directly linked to the processing of facial expressions-when the images were upright and they changed from a normal to a Thatcherized configuration. However, this release from adaptation was not evident when the faces were inverted. These results show that regions involved in processing facial expressions display a pronounced orientation sensitivity.

Orientation-sensitivity to facial features explains the Thatcher illusion.

The Thatcher illusion provides a compelling example of the perceptual cost of face inversion. The Thatcher illusion is often thought to result from a disruption to the processing of spatial relations between face features. Here, we show the limitations of this account and instead demonstrate that the effect of inversion in the Thatcher illusion is better explained by a disruption to the processing of purely local facial features. Using a matching task, we found that participants were able to discriminate normal and Thatcherized versions of the same face when they were presented in an upright orientation, but not when the images were inverted. Next, we showed that the effect of inversion was also apparent when only the eye region or only the mouth region was visible. These results demonstrate that a key component of the Thatcher illusion is to be found in orientation-specific encoding of the expressive features (eyes and mouth) of the face.

How neural representations of newly learnt faces change over time: Event-related brain potential evidence for overnight consolidation.

Previous experiments have shown that a brief encounter with a previously unfamiliar person leads to the establishment of new facial representations, which can be activated by completely novel pictures of the newly learnt face. The present study examined how stable such novel neural representations are over time, and, specifically, how they become consolidated within the first 24 h after learning. Using event-related brain potentials (ERPs) in a between-participants design, we demonstrate that clear face familiarity effects in the occipito-temporal N250 are evident immediately after learning. These effects then undergo change, with a nearly complete absence of familiarity-related ERP differences 4 h after the initial encounter. Critically, 24 h after learning, the original familiarity effect re-emerges. These findings suggest that the neural correlates of novel face representations are not stable over time but change during the first day after learning. The resulting pattern of change is consistent with a process of consolidation.

Clinical correlates of verbal aggression, physical aggression and inappropriate sexual behaviour after brain injury.

PRIMARY OBJECTIVE: To explore the relationships between verbal aggression, physical aggression and inappropriate sexual behaviour following acquired brain injury. RESEARCH DESIGN: Multivariate statistical modelling of observed verbal aggression, physical aggression and inappropriate sexual behaviour utilizing demographic, pre-morbid, injury-related and neurocognitive predictors. METHODS AND PROCEDURES: Clinical records of 152 participants with acquired brain injury were reviewed, providing an important data set as disordered behaviours had been recorded at the time of occurrence with the Brain Injury Rehabilitation Trust (BIRT) Aggression Rating Scale and complementary measures of inappropriate sexual behaviour. Three behavioural components (verbal aggression, physical aggression and inappropriate sexual behaviour) were identified and subjected to separate logistical regression modelling in a sub-set of 77 participants. MAIN OUTCOMES AND RESULTS: Successful modelling was achieved for both verbal and physical aggression (correctly classifying 74% and 65% of participants, respectively), with use of psychotropic medication and poorer verbal function increasing the odds of aggression occurring. Pre-morbid history of aggression predicted verbal but not physical aggression. No variables predicted inappropriate sexual behaviour. CONCLUSIONS: Verbal aggression, physical aggression and inappropriate sexual behaviour following acquired brain injury appear to reflect separate clinical phenomena rather than general behavioural dysregulation. Clinical markers that indicate an increased risk of post-injury aggression were not related to inappropriate sexual behaviour.