Functional Specificity In Eye Gaze Processing: Evidence From Developmental Prosopagnosia

SummaryHumans show a remarkable ability to discriminate others' gaze direction, even though a given direction can be conveyed by many physically dissimilar configurations of different eye positions and head views. For example, eye contact can be signaled by a rightward glance in a left-turned head or by direct gaze in a front-facing head. Such acute gaze discrimination implies considerable perceptual invariance. Previous human research found that superior temporal sulcus (STS) responds preferentially to gaze shifts [1], but the underlying representation that supports such general responsiveness remains poorly understood. Using multivariate pattern analysis (MVPA) of human functional magnetic resonance imaging (fMRI) data, we tested whether STS contains a higher-order, head view-invariant code for gaze direction. The results revealed a finely graded gaze direction code in right anterior STS that was invariant to head view and physical image features. Further analyses revealed similar gaze effects in left anterior STS and precuneus. Our results suggest that anterior STS codes the direction of another's attention regardless of how this information is conveyed and demonstrate how high-level face areas carry out fine-grained, perceptually relevant discrimination through invariance to other face features.

Background: Previous studies have shown abnormal eye gaze perception in schizophrenia, associated with compromised social functioning. However, the neural mechanisms of altered gaze perception in schizophrenia remain unclear, limiting our ability to design effective interventions. This study aims to use dynamic causal modeling (DCM) of functional MRI time-series data to reveal aberrant dynamics between brain regions associated with eye gaze perception in schizophrenia. Methods: Twenty-five patients with schizophrenia or schizoaffective disorder (SZ) and 20 healthy controls (HC) completed a gaze perception task during BOLD fMRI. Participants viewed faces with different gaze angles and decided either the gaze direction (Gaze: “Looking at you?” yes/no) or gender of the face (Gender: male/female). Four nodes were identified as regions of interest for DCM as they showed differential activation between Gaze and Gender: secondary visual cortex (Vis), temporo-parietal junction (TPJ), anterior insula (aIns), and medial prefrontal cortex (mPFC). A bilinear model space was generated with these 4 nodes, as well as visual input of face, self-connections, bidirectional connections between nodes, and modulation of gaze on the connections. Results: Bayesian model selection revealed a winning model, in which Vis showed bottom-up influence on mPFC, which in turn had direct top-down influences on aIns and TPJ and indirect top-down influence on Vis through TPJ; attending to gaze modulated the Vis-mPFC and mPFC-TPJ connections. Group difference was observed in the Gaze modulation on the Vis-mPFC connection, such that attending to gaze inhibited the bottom-up connection from Vis to mPFC but this inhibition was weakened in SZ relative to HC. Conclusion: These findings suggest that when determining the self-referential nature of social information, it is critical to suppress stimulus-driven processing and rely more on conceptually-driven cognition formulated from past experience. A reduced ability to do so may underlie the abnormalities observed in eye gaze perception in schizophrenia.

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

Individuals with bipolar disorder demonstrate abnormal social function. Neuroimaging studies in bipolar disorder have shown functional abnormalities in neural circuitry supporting face emotion processing, but have not examined face identity processing, a key component of social function. We aimed to elucidate functional abnormalities in neural circuitry supporting face emotion and face identity processing in bipolar disorder. Twenty-seven individuals with bipolar disorder I currently euthymic and 27 healthy controls participated in an implicit face processing, block-design paradigm. Participants labeled color flashes that were superimposed on dynamically changing background faces comprising morphs either from neutral to prototypical emotion (happy, sad, angry and fearful) or from one identity to another identity depicting a neutral face. Whole-brain and amygdala region-of-interest (ROI) activities were compared between groups. There was no significant between-group difference looking across both emerging face emotion and identity. During processing of all emerging emotions, euthymic individuals with bipolar disorder showed significantly greater amygdala activity. During facial identity and also happy face processing, euthymic individuals with bipolar disorder showed significantly greater amygdala and medial prefrontal cortical activity compared with controls. This is the first study to examine neural circuitry supporting face identity and face emotion processing in bipolar disorder. Our findings of abnormally elevated activity in amygdala and medial prefrontal cortex (mPFC) during face identity and happy face emotion processing suggest functional abnormalities in key regions previously implicated in social processing. This may be of future importance toward examining the abnormal self-related processing, grandiosity and social dysfunction seen in bipolar disorder.

Rationale: Face expertise is a pivotal social skill. Developmental prosopagnosia (DP), i.e., the inability to recognize faces without a history of brain damage, affects about 2% of the general population, and is a renowned model system of the face-processing network. Within this network, the right Fusiform Face Area (FFA), is particularly involved in face identity processing and may therefore be a key element in DP. Neural representations within the FFA have been examined with Representational Similarity Analysis (RSA), a data-analytical framework in which multi-unit measures of brain activity are assessed with correlation analysis.Objectives: Our study intended to scrutinize modifications of FFA-activation during face encoding and maintenance based on RSA.Methods: Thirteen participants with DP (23–70 years) and 12 healthy control subjects (19–62 years) participated in a functional MRI study, including morphological MRI, a functional FFA-localizer and a modified Sternberg paradigm probing face memory encoding and maintenance. Memory maintenance of one, two, or four faces represented low, medium, and high memory load. We examined conventional activation differences in response to working memory load and applied RSA to compute individual correlation-matrices on the voxel level. Group correlation-matrices were compared via Donsker’s random walk analysis.Results: On the functional level, increased memory load entailed both a higher absolute FFA-activation level and a higher degree of correlation between activated voxels. Both aspects were deficient in DP. Interestingly, control participants showed a homogeneous degree of correlation for successful trials during the experiment. In DP-participants, correlation levels between FFA-voxels were significantly lower and were less sustained during the experiment. In behavioral terms, DP-participants performed poorer and had longer reaction times in relation to DP-severity. Furthermore, correlation levels were negatively correlated with reaction times for the most demanding high load condition.Conclusion: We suggest that participants with DP fail to generate robust and maintained neural representations in the FFA during face encoding and maintenance, in line with poorer task performance and prolonged reaction times. In DP, alterations of neural coding in the FFA might therefore explain curtailing in working memory and contribute to impaired long-term memory and mental imagery.

Previous research using averted (e.g., leftward or rightward) gaze indicates that gaze perception requires a focus of attention. However, direct gaze, compared with averted gaze, is processed in the brain preferentially and enhances cognitive functions. Thus, it is necessary to use direct gaze to investigate whether gaze perception is possible without focused attention. We conducted a dual-task paradigm in which attention was drawn away from gaze. Results showed performance on gaze-direction discrimination (direct vs. averted gaze) in the dual-task condition was only slightly lower than in the single-task condition; participants were able to discriminate direct from averted gaze without focusing their attention in a similar manner to when they did focus their attention. In contrast, when participants discriminated between averted gazes (leftward and rightward), performance dropped to near-chance levels. It was concluded that gaze perception does not require a focus of attention for direct gaze.

Previous research using averted (e.g., leftward or rightward) gaze indicates that gaze perception requires a focus of attention. However, direct gaze, compared with averted gaze, is processed in the brain preferentially and enhances cognitive functions. Thus, it is necessary to use direct gaze to investigate whether gaze perception is possible without focused attention. We conducted a dual-task paradigm in which attention was drawn away from gaze. Results showed performance on gaze-direction discrimination (direct vs. averted gaze) in the dual-task condition was only slightly lower than in the single-task condition; participants were able to discriminate direct from averted gaze without focusing their attention in a similar manner to when they did focus their attention. In contrast, when participants discriminated between averted gazes (leftward and rightward), performance dropped to near-chance levels. It was concluded that gaze perception does not require a focus of attention for direct gaze.

A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder

The meter of nursery rhymes: An application of the Halle-Keyser theory of meter

Facial identity recognition is one of the challenging problems in the domain of computer vision. Facial identity comprises the facial attributes of a person’s face ranging from age progression, gender, hairstyle, etc. Manipulating facial attributes such as changing the gender, hairstyle, expressions, and makeup changes the entire facial identity of a person which is often used by law offenders to commit crimes. Leveraging the deep learning-based approaches, this work proposes a one-step solution for facial attribute manipulation and detection leading to facial identity recognition in few-shot and traditional scenarios. As a first step towards performing facial identity recognition, we created the Facial Attribute Manipulation Detection (FAM) Dataset which consists of twenty unique identities with thirty-eight facial attributes generated by the StyleGAN3 inversion. The Facial Attribute Detection (FAM) Dataset has 11,560 images richly annotated in YOLO format. To perform facial attribute and identity detection, we developed the Spatial Transformer Block (STB) and Squeeze-Excite Spatial Pyramid Pooling (SE-SPP)-based Tiny YOLOv7 model and proposed as FIR-Tiny YOLOv7 (Facial Identity Recognition-Tiny YOLOv7) model. The proposed model is an improvised variant of the Tiny YOLOv7 model. For facial identity recognition, the proposed model achieved 10.0% higher mAP in the one-shot scenario, 30.4% higher mAP in the three-shot scenario, 15.3% higher mAP in the five-shot scenario, and 0.1% higher mAP in the traditional 70% − 30% split scenario as compared to the Tiny YOLOv7 model. The results obtained with the proposed model are promising for general facial identity recognition under varying facial attribute manipulation.

The ability to recognise the identity and expressions of faces varies among humans and can be problematic in conditions such as autism, developmental prosopagnosia, and acquired prosopagnosia. Studies have examined whether training can improve this skill but these differ in the cognitive operations targeted, the technical details of training, and the methods of evaluation. In typical subjects the matching of unfamiliar faces is notoriously unreliable, which is a challenge in forensic settings, and training appears to have minimal effects of 5–10% that are limited to those who are poorer than average to begin. With autism spectrum disorders (ASD)s there has been training of the recognition of facial expressions and face identity, which again leads to modest perceptual gains, with no evidence that this improves social functioning. A variety of perceptual and mnemonic rehabilitative approaches have been applied to prosopagnosia. With acquired prosopagnosia these have involved mainly case studies, though one group study found that perceptual learning for faces improved the discriminative ability of these patients. Three group studies of developmental prosopagnosia have reported gains with perceptual training, which were more evident in participants with more severe deficits. Future work is needed to see if these modest but encouraging results can be enhanced with adjunctive measures that promote neural plasticity and learning.

The current study investigated if deficits in processing emotional expression affect facial identity processing and vice versa in children with autism spectrum disorder. Children with autism and IQ and age matched typically developing children classified faces either by emotional expression, thereby ignoring facial identity or by facial identity disregarding emotional expression. Typically developing children processed facial identity independently from facial expressions but processed facial expressions in interaction with identity. Children with autism processed both facial expression and identity independently of each other. They selectively directed their attention to one facial parameter despite variations in the other. Results indicate that there is no interaction in processing facial identity and emotional expression in autism spectrum disorder.

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.

Regions of the occipital and temporal lobes, including a region in the fusiform gyrus (FG), have been proposed to constitute a "core" visual representation system for faces, in part because they show face selectivity and face repetition suppression. But recent fMRI studies of developmental prosopagnosics (DPs) raise questions about whether these measures relate to face processing skills. Although DPs manifest deficient face processing, most studies to date have not shown unequivocal reductions of functional responses in the proposed core regions. We scanned 15 DPs and 15 non-DP control participants with fMRI while employing factor analysis to derive behavioral components related to face identification or other processes. Repetition suppression specific to facial identities in FG or to expression in FG and STS did not show compelling relationships with face identification ability. However, we identified robust relationships between face selectivity and face identification ability in FG across our sample for several convergent measures, including voxel-wise statistical parametric mapping, peak face selectivity in individually defined "fusiform face areas" (FFAs), and anatomical extents (cluster sizes) of those FFAs. None of these measures showed associations with behavioral expression or object recognition ability. As a group, DPs had reduced face-selective responses in bilateral FFA when compared with non-DPs. Individual DPs were also more likely than non-DPs to lack expected face-selective activity in core regions. These findings associate individual differences in face processing ability with selectivity in core face processing regions. This confirms that face selectivity can provide a valid marker for neural mechanisms that contribute to face identification ability.

Results on brain imaging studies have led to a better understanding of the neural circuits involved in social cognition and its implication in autism spectrum disorders(ASD). It has been shown that the superior temporal sulcus(STS)is highly implicated in social processes, from perception of socially relevant information, such as body movements or eye gaze, to more complex social cognition processes. Furthermore, several multimodal brain imaging results point to anatomo-functional abnormalities in the STS in both children and adults with ASD. These results are highly consistent with social impairments in ASD, among which eye gaze perception is particularly relevant. Gaze abnormalities can now be objectively measured using eye-tracking methodology, leading to a better characterization of social perception impairments in autism. Moreover, these gaze abnormalities have been associated with STS abnormalities in ASD. Based on these results, our hypothesis is that anatomo-functional anomalies in the STS occurring early across brain development could constitute the first step in the cascade of neural dysfunction underlying autism. In the present work, we'll review recent data of STS contribution to normal social cognition and it's implication in autism.