Neural basis of prosopagnosia: an fMRI study

Brain imaging research has identified at least two regions in human extrastriate cortex responding selectively to faces. One of these is located in the mid-fusiform gyrus (FFA), the other in the inferior occipital gyrus (IOG). We studied activation of these areas using fMRI in three individuals with severely impaired face recognition (one pure developmental and two childhood prosopagnosics). None of the subjects showed the normal pattern of higher fMRI activity to faces than to objects in the FFA and IOG or elsewhere. Moreover, in two of the patients, faces and objects produced similar activations in the regions corresponding to where the FFA and IOG are found in normal subjects. Our study casts light on the important role of FFA and IOG in the network of areas involved in face recognition, and indicates limits of brain plasticity.     

Direct structural connections between voice- and face-recognition areas

Currently, there are two opposing models for how voice and face information is integrated in the human brain to recognize person identity. The conventional model assumes that voice and face information is only combined at a supramodal stage (Bruce and Young, 1986; Burton et al., 1990; Ellis et al., 1997). An alternative model posits that areas encoding voice and face information also interact directly and that this direct interaction is behaviorally relevant for optimizing person recognition (von Kriegstein et al., 2005; von Kriegstein and Giraud, 2006). To disambiguate between the two different models, we tested for evidence of direct structural connections between voice- and face-processing cortical areas by combining functional and diffusion magnetic resonance imaging. We localized, at the individual subject level, three voice-sensitive areas in anterior, middle, and posterior superior temporal sulcus (STS) and face-sensitive areas in the fusiform gyrus [fusiform face area (FFA)]. Using probabilistic tractography, we show evidence that the FFA is structurally connected with voice-sensitive areas in STS. In particular, our results suggest that the FFA is more strongly connected to middle and anterior than to posterior areas of the voice-sensitive STS. This specific structural connectivity pattern indicates that direct links between face- and voice-recognition areas could be used to optimize human person recognition.     

Abnormal Activation of the Social Brain Network in Children with Autism Spectrum Disorder: An fMRI Study

Objective

The aim of this study is to investigate abnormal findings of social brain network in Korean children with autism spectrum disorder (ASD) compared with typically developing children (TDC).

Methods

Functional magnetic resonance imaging (fMRI) was performed to examine brain activations during the processing of emotional faces (happy, fearful, and neutral) in 17 children with ASD, 24 TDC.

Results

When emotional face stimuli were given to children with ASD, various areas of the social brain relevant to social cognition showed reduced activation. Specifically, ASD children exhibited less activation in the right amygdala (AMY), right superior temporal sulcus (STS) and right inferior frontal gyrus (IFG) than TDC group when fearful faces were shown. Activation of left insular cortex and right IFG in response to happy faces was less in the ASD group. Similar findings were also found in left superior insular gyrus and right insula in case of neutral stimulation.

Conclusion

These findings suggest that children with ASD have different processing of social and emotional experience at the neural level. In other words, the deficit of social cognition in ASD could be explained by the deterioration of the capacity for visual analysis of emotional faces, the subsequent inner imitation through mirror neuron system (MNS), and the ability to transmit it to the limbic system and to process the transmitted emotion.     

Neural responses to rigidly moving faces displaying shifts in social attention investigated with fMRI and MEG

A widely adopted neural model of face perception (Haxby, Hoffman, & Gobbini, 2000) proposes that the posterior superior temporal sulcus (STS) represents the changeable features of a face, while the face-responsive fusiform gyrus (FFA) encodes invariant aspects of facial structure. ‘Changeable features’ of a face can include rigid and non-rigid movements. The current study investigated neural responses to rigid, moving faces displaying shifts in social attention. Both functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) were used to investigate neural responses elicited when participants viewed video clips in which actors made a rigid shift of attention, signalled congruently from both the eyes and head. These responses were compared to those elicited by viewing static faces displaying stationary social attention information or a scrambled video displaying directional motion. Both the fMRI and MEG analyses demonstrated heightened responses along the STS to turning heads compared to static faces or scrambled movement conditions. The FFA responded to both turning heads and static faces, showing only a slight increase in response to the dynamic stimuli. These results establish the applicability of the Haxby model to the perception of rigid face motions expressing changes in social attention direction. Furthermore, the MEG beamforming analyses found an STS response in an upper frequency band (30-80 Hz) which peaked in the right anterior region. These findings, derived from two complementary neuroimaging techniques, clarify the contribution of the STS during the encoding of rigid facial action patterns of social attention, emphasising the role of anterior sulcal regions alongside previously observed posterior areas.     

Is the fusiform face area specialized for faces, individuation, or expert individuation?

Several brain imaging studies have identified a region of fusiform gyrus (FG) that responds more strongly to faces than common objects. The precise functional role of this fusiform face area (FFA) is, however, a matter of dispute. We sought to distinguish among three hypotheses concerning FFA function: face specificity, individuation, and expert individuation. According to the face-specificity hypothesis, the FFA is specialized for face processing. Alternatively, the FFA may be specialized for individuating visually similar items within a category (the individuation hypothesis) or for individuating within categories with which a person has expertise (the expert-individuation hypothesis). Our results from two experiments supported the face-specificity hypothesis. Greater FFA activation to faces than Lepidoptera, another homogeneous object class, occurred during both free viewing and individuation, with similar FFA activation to Lepidoptera and common objects (Experiment 1). Furthermore, during individuation of Lepidoptera, 83% of activated FG voxels were outside the face FG region and only 15% of face FG voxels were activated. This pattern of results suggests that distinct areas may individuate faces and Lepidoptera. In Experiment 2, we tested Lepidoptera experts using the same experimental design. Again, the results supported the face-specificity hypothesis. Activation to faces in the FFA was greater than to both Lepidoptera and objects with little overlap between FG areas activated by faces and Lepidoptera. Our results suggest that distinct populations of neurons in human FG may be tuned to the features needed to individuate the members of different object classes, as has been reported in monkey inferotemporal cortex, and that the FFA contains neurons tuned for individuating faces.     

Neuroanatomical and neurofunctional markers of social cognition in autism spectrum disorder

Social impairments in autism spectrum disorder (ASD), a hallmark feature of its diagnosis, may underlie specific neural signatures that can aid in differentiating between those with and without ASD. To assess common and consistent patterns of differences in brain responses underlying social cognition in ASD, this study applied an activation likelihood estimation (ALE) meta‐analysis to results from 50 neuroimaging studies of social cognition in children and adults with ASD. In addition, the group ALE clusters of activation obtained from this was used as a social brain mask to perform surface‐based cortical morphometry (SBM) in an empirical structural MRI dataset collected from 55 ASD and 60 typically developing (TD) control participants. Overall, the ALE meta‐analysis revealed consistent differences in activation in the posterior superior temporal sulcus at the temporoparietal junction, middle frontal gyrus, fusiform face area (FFA), inferior frontal gyrus (IFG), amygdala, insula, and cingulate cortex between ASD and TD individuals. SBM analysis showed alterations in the thickness, volume, and surface area in individuals with ASD in STS, insula, and FFA. Increased cortical thickness was found in individuals with ASD, the IFG. The results of this study provide functional and anatomical bases of social cognition abnormalities in ASD by identifying common signatures from a large pool of neuroimaging studies. These findings provide new insights into the quest for a neuroimaging‐based marker for ASD. Hum Brain Mapp 37:3957–3978, 2016. © 2016 Wiley Periodicals, Inc.     

Different fusiform activity to stranger and personally familiar faces in shy and social adults

Abstract

Although shyness is associated with deficits in different aspects of face processing including face recognition and facial emotions, we know relatively little about the neural correlates of face processing among individuals who are shy. Here we show reduced activation to stranger faces among shy adults in a key brain area involved in face processing. Event-related functional magnetic resonance imaging scans were acquired on 12 shy and 12 social young adults during the rapid presentation of stranger and personally familiar neutral faces. Shy adults exhibited significantly less bilateral activation in the fusiform face area (FFA) in response to stranger faces and significantly greater bilateral activation in the same region to personally familiar faces than their social counterparts. Shy adults also exhibited significantly greater right amygdala activation in response to stranger faces than social adults. Among social adults, stranger faces elicited greater FFA activation than personally familiar faces. Findings suggest that there are distinct patterns of neural activation in the FFA in response to viewing stranger and personally familiar faces among shy and social adults.     

The Role of Face Familiarity in Eye Tracking of Faces by Individuals with Autism Spectrum Disorders

It has been shown that individuals with autism spectrum disorders (ASD) demonstrate normal activation in the fusiform gyrus when viewing familiar, but not unfamiliar faces. The current study utilized eye tracking to investigate patterns of attention underlying familiar versus unfamiliar face processing in ASD. Eye movements of 18 typically developing participants and 17 individuals with ASD were recorded while passively viewing three face categories: unfamiliar non-repeating faces, a repeating highly familiar face, and a repeating previously unfamiliar face. Results suggest that individuals with ASD do not exhibit more normative gaze patterns when viewing familiar faces. A second task assessed facial recognition accuracy and response time for familiar and novel faces. The groups did not differ on accuracy or reaction times.     

Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders

Schizophrenia and autism both feature significant impairments in social cognition and social functioning, but the specificity and mechanisms of these deficits remain unknown. Recent research suggests that social cognitive deficits in both disorders may arise from dysfunctions in the neural systems that underlie social cognition. We explored the neural activation of discrete brain regions implicated in social cognitive and face processing in schizophrenia subgroups and autism spectrum disorders during complex social judgments of faces. Twelve individuals with autism spectrum disorders (ASD), 12 paranoid individuals with schizophrenia (P-SCZ), 12 non-paranoid individuals with schizophrenia (NP-SCZ), and 12 non-clinical healthy controls participated in this cross sectional study. Neural activation, as indexed by blood oxygenation level dependent (BOLD) contrast, was measured in a priori regions of interest while individuals rated faces for trustworthiness. All groups showed significant activation of a social cognitive network including the amygdala, fusiform face area (FFA), superior temporal sulcus (STS), and ventrolateral prefrontal cortex (VLPFC) while completing a task of complex social cognition (i.e. trustworthiness judgments). ASD and P-SCZ individuals showed significantly reduced neural activation in the right amygdala, FFA, and left VLPFC as compared to controls and in the left VLPFC as compared to NP-SCZ individuals during this task. These findings lend support to models hypothesizing well-defined neural substrates of social cognition and suggest a specific neural mechanism that may underlie social cognitive impairments in both autism and paranoid schizophrenia.     

Attention to emotion modulates fMRI activity in human right superior temporal sulcus

A parallel neural network has been proposed for processing various types of information conveyed by faces including emotion. Using functional magnetic resonance imaging (fMRI), we tested the effect of the explicit attention to the emotional expression of the faces on the neuronal activity of the face-responsive regions. Delayed match to sample procedure was adopted. Subjects were required to match the visually presented pictures with regard to the contour of the face pictures, facial identity, and emotional expressions by valence (happy and fearful expressions) and arousal (fearful and sad expressions). Contour matching of the non-face scrambled pictures was used as a control condition. The face-responsive regions that responded more to faces than to non-face stimuli were the bilateral lateral fusiform gyrus (LFG), the right superior temporal sulcus (STS), and the bilateral intraparietal sulcus (IPS). In these regions, general attention to the face enhanced the activities of the bilateral LFG, the right STS, and the left IPS compared with attention to the contour of the facial image. Selective attention to facial emotion specifically enhanced the activity of the right STS compared with attention to the face per se. The results suggest that the right STS region plays a special role in facial emotion recognition within distributed face-processing systems. This finding may support the notion that the STS is involved in social perception.     

Time course of gamma‐band oscillation associated with face processing in the inferior occipital gyrus and fusiform gyrus: A combined fMRI and MEG study

Debate continues over whether the inferior occipital gyrus (IOG) or the fusiform gyrus (FG) represents the first stage of face processing and what role these brain regions play. We investigated this issue by combining functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) in normal adults. Participants passively observed upright and inverted faces and houses. First, we identified the IOG and FG as face‐specific regions using fMRI. We applied beamforming source reconstruction and time–frequency analysis to MEG source signals to reveal the time course of gamma‐band activations in these regions. The results revealed that the right IOG showed higher gamma‐band activation in response to upright faces than to upright houses at 100 ms from the stimulus onset. Subsequently, the right FG showed greater gamma‐band response to upright faces versus upright houses at around 170 ms. The gamma‐band activation in the right IOG and right FG was larger in response to inverted faces than to upright faces at the later time window. These results suggest that (1) the gamma‐band activities occurs rapidly first in the IOG and next in the FG and (2) the gamma‐band activity in the right IOG at later time stages is involved in configuration processing for faces. Hum Brain Mapp 38:2067–2079, 2017. © 2017 Wiley Periodicals, Inc.     

Face processing changes in normal aging revealed by fMRI adaptation

We investigated the neural correlates of facial processing changes in healthy aging using fMRI and an adaptation paradigm. In the scanner, participants were successively presented with faces that varied in identity, viewpoint, both, or neither and performed a head size detection task independent of identity or viewpoint. In right fusiform face area (FFA), older adults failed to show adaptation to the same face repeatedly presented in the same view, which elicited the most adaptation in young adults. We also performed a multivariate analysis to examine correlations between whole-brain activation patterns and behavioral performance in a face-matching task tested outside the scanner. Despite poor neural adaptation in right FFA, high-performing older adults engaged the same face-processing network as high-performing young adults across conditions, except the one presenting a same facial identity across different viewpoints. Low-performing older adults used this network to a lesser extent. Additionally, high-performing older adults uniquely recruited a set of areas related to better performance across all conditions, indicating age-specific involvement of this added network. This network did not include the core ventral face-processing areas but involved the left inferior occipital gyrus, frontal, and parietal regions. Although our adaptation results show that the neuronal representations of the core face-preferring areas become less selective with age, our multivariate analysis indicates that older adults utilize a distinct network of regions associated with better face matching performance, suggesting that engaging this network may compensate for deficiencies in ventral face processing regions.     

A functional MRI study of face recognition in patients with prosopagnosia.

An fMRI investigation was conducted to determine whether patients with impaired face recognition, a deficit known as prosopagnosia, would show functional activation in the fusiform gyrus, the neural substrate for face processing, when viewing faces. While the patients did show activation in the fusiform gyrus, with significantly more voxels in posterior areas than their control subjects, this activation was not sufficient for face processing. In one of the patients, the posterior activation was particularly evident in the left hemisphere, which is thought to be involved in feature-based strategies of face perception. We conclude that an increased reliance on feature-based processing in prosopagnosia leads to a recruitment of neurons in posterior regions of the fusiform gyrus, regions that are not ideally suited for processing faces.     

Regional brain response to faces of humans and dogs

The extent to which the brain regions associated with face processing are selective for that specific function remains controversial. In addition, little is known regarding the extent to which face-responsive brain regions are selective for human faces. To study regional selectivity of face processing, we used functional magnetic resonance imaging to examine whole brain activation in response to human faces, dog faces, and houses. Fourteen healthy right-handed volunteers participated in a passive viewing, blocked experiment. Results indicate that the lateral fusiform gyrus (Brodmann's area 37) responds maximally to both dog and human faces when compared with other sites, followed by the middle/inferior occipital gyrus (BA 18/19). Sites that were activated by houses versus dog and human faces included the medial fusiform gyrus (BA 19/37), the posterior cingulate (BA 30), and the superior occipital gyrus (BA 19). The only site that displayed significant differences in activation between dog and human faces was the lingual/medial fusiform gyrus. In this site, houses elicited the strongest activation, followed by dog faces, while the response to human faces was negligible and did not differ from fixation. The parahippocampal gyrus/amygdala was the sole site that displayed significant activation to human faces, but not to dog faces or houses.     

The anatomic basis of the right face-selective N170 IN acquired prosopagnosia: a combined ERP/fMRI study

The N170 waveform is larger over posterior temporal cortex when healthy subjects view faces than when they view other objects. Source analyses have produced mixed results regarding whether this effect originates in the fusiform face area (FFA), lateral occipital cortex, or superior temporal sulcus (STS), components of the core face network. In a complementary approach, we assessed the face-selectivity of the right N170 in five patients with acquired prosopagnosia, who also underwent structural and functional magnetic resonance imaging. We used a non-parametric bootstrap procedure to perform single-subject analyses, which reliably confirmed N170 face-selectivity in each of 10 control subjects. Anterior temporal lesions that spared the core face network did not affect the face-selectivity of the N170. A face-selective N170 was also present in another subject who had lost only the right FFA. However, face-selectivity was absent in two patients with lesions that eliminated the occipital face area (OFA) and FFA, sparing only the STS. Thus while the right FFA is not necessary for the face-selectivity of the N170, neither is the STS sufficient. We conclude that the face-selective N170 in prosopagnosia requires residual function of at least two components of the core face-processing network.     

Altered fusiform connectivity during processing of fearful faces in social anxiety disorder

Social anxiety disorder (SAD) has been associated with hyper-reactivity in limbic brain regions like the amygdala, both during symptom provocation and emotional face processing tasks. In this functional magnetic resonance imaging study we sought to examine brain regions implicated in emotional face processing, and the connectivity between them, in patients with SAD (n=14) compared with healthy controls (n=12). We furthermore aimed to relate brain reactivity and connectivity to self-reported social anxiety symptom severity. SAD patients exhibited hyper-reactivity in the bilateral fusiform gyrus in response to fearful faces, as well as greater connectivity between the fusiform gyrus and amygdala, and decreased connectivity between the fusiform gyrus and ventromedial prefrontal cortex. Within the SAD group, social anxiety severity correlated positively with amygdala reactivity to emotional faces, amygdala-fusiform connectivity and connectivity between the amygdala and superior temporal sulcus (STS). These findings point to a pivotal role for the fusiform gyrus in SAD neuropathology, and further suggest that altered amygdala-fusiform and amygdala-STS connectivity could underlie previous findings of aberrant socio-emotional information processing in this anxiety disorder.     

The functional architecture for face-processing expertise: FMRI evidence of the developmental trajectory of the core and the extended face systems

Expertise in processing faces is a cornerstone of human social interaction. However, the developmental course of many key brain regions supporting face preferential processing in the human brain remains undefined. Here, we present findings from an FMRI study using a simple viewing paradigm of faces and objects in a continuous age sample covering the age range from 6 years through adulthood. These findings are the first to use such a sample paired with whole-brain FMRI analyses to investigate development within the core and extended face networks across the developmental spectrum from middle childhood to adulthood. We found evidence, albeit modest, for a developmental trend in the volume of the right fusiform face area (rFFA) but no developmental change in the intensity of activation. From a spatial perspective, the middle portion of the right fusiform gyrus most commonly found in adult studies of face processing was increasingly likely to be included in the FFA as age increased to adulthood. Outside of the FFA, the most striking finding was that children hyperactivated nearly every aspect of the extended face system relative to adults, including the amygdala, anterior temporal pole, insula, inferior frontal gyrus, anterior cingulate gyrus, and parietal cortex. Overall, the findings suggest that development is best characterized by increasing modulation of face-sensitive regions throughout the brain to engage only those systems necessary for task requirements.     

Neurophysiological studies in autism spectrum disorders--comparison with those in schizophrenia

There have been reports that autism spectrum disorders (ASD) share common symptoms with schizophrenia. Several imaging studies showed the overlap of the impaired brain circuit in ASD and schizophrenia. Accordingly, differential diagnoses between adult ASD and schizophrenia without positive symptoms are sometimes difficult. We examined whether they show common results in functional MRI studies involving viewing photos of different facial expressions, such as angry, happy, sad, and neutral faces. We also examined oculomotor tasks that consist of saccadic and smooth pursuit eye movements in the two groups of patients. In fMRI studies, 15 schizophrenia patients (8 females) and 15 ASD patients (9 females) who met the criteria for DSM-IV participated. For the typically developed (TD) control group, 15 subjects (6 females) with no history of neurological or psychiatric disorders were recruited from the community. There was no significant difference in ages and sex ratios among these three groups. ANOVA comparison indicated that the ASD group showed significantly reduced activity in the right fusiform gyrus (FG) on viewing sad, happy, and neutral expressions but higher activity in the right mirror neuron system in the frontal cortex during viewing an angry expression. These results suggest a disturbance of the FG for face recognition and an excessive reaction to angry faces in ASD subjects. On the other hand, schizophrenics showed significantly reduced activation in widespread cortical areas, including the frontal, parietal, temporal, and occipital cortex, in comparison with TD and ASD individuals. We also examined voluntary control of saccadic and smooth pursuit eye movements in 13 adult subjects aged 20-35 with ASD (5 females) and compared the results with the performance of 13 TDs. Saccadic and smooth pursuit eye movements were recorded using an infrared system. Compared with TDs, 38% of the ASD subjects showed higher error rates in the anti-saccade task. However, in horizontal sinusoidal smooth pursuit, they showed normal gains. On the other hand, about 70% of 99 schizophrenics showed abnormalities in the antisaccade tasks. In the smooth pursuit task, 60-70% of schizophrenics showed a lower gain than controls. In this study, although all of the ASD subjects were adults and the number examined was relatively small, their abnormalities in fMRI and eye movement tasks were milder than those of schizophrenics.     

Here's looking at you, kid: neural systems underlying face and gaze processing in fragile X syndrome

BACKGROUND: Children with fragile X syndrome (fraX) are at risk for manifesting abnormalities in social function that overlap with features of autism and social anxiety disorder. In this study, we analyzed brain activation in response to face and gaze stimuli to better understand neural functioning associated with social perception in fraX. METHODS: Eleven female subjects with fraX, aged 10 to 22 years, were compared with age-matched female control subjects. Photographs of forward-facing and angled faces, each having direct and averted gaze (4 types of stimuli), were presented in an event-related design during functional magnetic resonance imaging. Subjects were instructed to determine the direction of gaze for each photograph. Activation in brain regions known to respond to face and gaze stimuli, the fusiform gyrus (FG) and superior temporal sulcus (STS), were compared between groups to isolate neural abnormalities in the perception of directed social stimuli. RESULTS: The fraX subjects had decreased accuracy in determining the direction of gaze compared with controls. Region of interest analysis of the FG revealed a significant interaction between diagnostic group and face orientation. Specifically, control subjects had greater FG activation to forward than to angled faces, whereas fraX subjects had no difference in FG activation to forward and angled faces. Controls showed greater left STS activation to all stimuli compared with fraX subjects. CONCLUSIONS: Our results suggest that gaze aversion in fraX subjects is related to decreased specialization of the FG in the perception of face orientation. Decreased STS activation in fraX suggests aberrant processing of gaze. These data suggest that gaze aversion in fraX may be related to dysfunction of neural systems underlying both face and gaze processing.     

Are face-responsive regions selective only for faces?

To examine the specificity of face-responsive regions for face processing, we used fMRI to measure the response of the fusiform gyrus and the superior temporal sulcus (STS) to pictures of human faces, animals, faceless animals, and houses. Results indicate that faces, animals, and faceless animals all elicited greater activity than houses, and had identical peaks of activation in the lateral fusiform gyrus, bilaterally, and in the right posterior STS. Moreover, within the lateral fusiform gyrus the responses to faces, animals and faceless animals were all greater than the responses to these stimuli in the medial aspect of the fusiform gyrus, a region that responds more strongly to other objects (e.g. houses). These findings suggest that the neural representation of animals in the fusiform gyrus and the posterior STS relies strongly on the same neural substrates that represent faces.