Bilateral Fusiform Face Area Research Articles

Investigating the neural effects of typicality and predictability for face and object stimuli.

The brain calibrates itself based on the past stimulus diet, which makes frequently observed stimuli appear as typical (as opposed to uncommon stimuli, which appear as distinctive). Based on predictive processing theory, the brain should be more "prepared" for typical exemplars, because these contain information that has been encountered frequently, allowing it to economically represent items of that category. Thus, one could ask whether predictability and typicality of visual stimuli interact, or rather act in an additive manner. We adapted the design by Egner and colleagues (2010), who used cues to induce expectations about stimulus category (face vs. chair) occurrence during an orthogonal inversion detection task. We measured BOLD responses with fMRI in 35 participants. First, distinctive stimuli always elicited stronger responses than typical ones in all ROIs, and our whole-brain directional contrasts for the effects of typicality and distinctiveness converge with previous findings. Second and importantly, we could not replicate the interaction between category and predictability reported by Egner et al. (2010), which casts doubt on whether cueing designs are ideal to elicit reliable predictability effects. Third, likely as a consequence of the lack of predictability effects, we found no interaction between predictability and typicality in any of the four tested regions (bilateral fusiform face areas, lateral occipital complexes) when considering both categories, nor in the whole brain. We discuss the issue of replicability in neuroscience and sketch an agenda for how future studies might address the same question.

Neurobiological correlates and attenuated positive social intention attribution during laughter perception associated with degree of autistic traits

Laughter plays an important role in group formation, signaling social belongingness by indicating a positive or negative social intention towards the receiver. In adults without autism, the intention of laughter can be correctly differentiated without further contextual information. In autism spectrum disorder (ASD), however, differences in the perception and interpretation of social cues represent a key characteristic of the disorder. Studies suggest that these differences are associated with hypoactivation and altered connectivity among key nodes of the social perception network. How laughter, as a multimodal nonverbal social cue, is perceived and processed neurobiologically in association with autistic traits has not been assessed previously. We investigated differences in social intention attribution, neurobiological activation, and connectivity during audiovisual laughter perception in association with the degree of autistic traits in adults [N = 31, Mage (SD) = 30.7 (10.0) years, nfemale = 14]. An attenuated tendency to attribute positive social intention to laughter was found with increasing autistic traits. Neurobiologically, autistic trait scores were associated with decreased activation in the right inferior frontal cortex during laughter perception and with attenuated connectivity between the bilateral fusiform face area with bilateral inferior and lateral frontal, superior temporal, mid-cingulate and inferior parietal cortices. Results support hypoactivity and hypoconnectivity during social cue processing with increasing ASD symptoms between socioemotional face processing nodes and higher-order multimodal processing regions related to emotion identification and attribution of social intention. Furthermore, results reflect the importance of specifically including signals of positive social intention in future studies in ASD.

Multiple-stage impairments of unfamiliar face learning in developmental prosopagnosia: Evidence from fMRI repetition suppression and multi-voxel pattern stability

Individuals with developmental prosopagnosia (DP) are characterized by severe face recognition deficits, yet it remains unknown how they are hindered in the process of unfamiliar face learning. Here we tracked the changes of neural activation during unfamiliar face repetition in DP with fMRI to reveal their neural deficits in learning unfamiliar faces. At the perceptual level, we found that the bilateral fusiform face area (FFA) in individuals with DP showed attenuated repetition suppression for faces, suggesting an inefficient perceptual analysis for learned faces. At the mnemonic level, individuals with DP showed decreased multi-voxel pattern stability for repeated faces in bilateral medial temporal lobe (MTL), suggesting an unstable mnemonic representation for learned faces. In addition, resting-state functional connectivity between the FFA and MTL was also disrupted in individuals with DP. Finally, the MTL's unstable mnemonic representation was associated with the impaired face recognition performance in DP. In sum, our study provides evidence that individuals with DP showed multi-stage neural deficits in unfamiliar face learning and sheds new light on how unfamiliar faces are learned in normal population.

Correlates of individual voice and face preferential responses during resting state

Human nonverbal social signals are transmitted to a large extent by vocal and facial cues. The prominent importance of these cues is reflected in specialized cerebral regions which preferentially respond to these stimuli, e.g. the temporal voice area (TVA) for human voices and the fusiform face area (FFA) for human faces. But it remained up to date unknown whether there are respective specializations during resting state, i.e. in the absence of any cues, and if so, whether these representations share neural substrates across sensory modalities. In the present study, resting state functional connectivity (RSFC) as well as voice- and face-preferential activations were analysed from functional magnetic resonance imaging (fMRI) data sets of 60 healthy individuals. Data analysis comprised seed-based analyses using the TVA and FFA as regions of interest (ROIs) as well as multi voxel pattern analyses (MVPA). Using the face- and voice-preferential responses of the FFA and TVA as regressors, we identified several correlating clusters during resting state spread across frontal, temporal, parietal and occipital regions. Using these regions as seeds, characteristic and distinct network patterns were apparent with a predominantly convergent pattern for the bilateral TVAs whereas a largely divergent pattern was observed for the bilateral FFAs. One region in the anterior medial frontal cortex displayed a maximum of supramodal convergence of informative connectivity patterns reflecting voice- and face-preferential responses of both TVAs and the right FFA, pointing to shared neural resources in supramodal voice and face processing. The association of individual voice- and face-preferential neural activity with resting state connectivity patterns may support the perspective of a network function of the brain beyond an activation of specialized regions.

Separate and Shared Neural Basis of Face Memory and Face Perception in Developmental Prosopagnosia.

Developmental prosopagnosia (DP), also known as face blindness, is a cognitive disorder with a severe deficit in recognizing faces. However, the heterogeneous nature of DP leads to a longstanding debate on which stages the deficit occurs, face perception (e.g., matching two consecutively presented faces) or face memory (e.g., matching a face to memorized faces). Here, we used the individual difference approach with functional magnetic resonance imaging to explore the neural substrates of DPs’ face perception and face memory that may illuminate DPs’ heterogeneity. Specifically, we measured the behavioral performance of face perception and face memory in a large sample of individuals suffering DP (N = 64) and then associated the behavioral performance with their face-selective neural responses in the core face network (CFN) and the extended face network (EFN), respectively. Behaviorally, we found that DP individuals were impaired in both face perception and face memory; however, there was only a weak correlation between the performances of two tasks. Consistent with this observation, the neural correlate of DPs’ performance in face memory task was localized in the bilateral fusiform face area, whereas DPs’ performance in face perception task was correlated with the face selectivity in the right posterior superior temporal sulcus, suggesting that the neural substrates in the CFN for face memory and face perception were separate in DP. In contrast, shared neural substrates of deficits in face perception and face memory tasks were identified in the EFN, including the right precuneus and the right orbitofrontal cortex. In summary, our study provides one of the first empirical evidence that the separate and shared neural substrates of face perception and face memory were identified in the CFN and EFN, respectively, which may help illuminating DP’s heterogeneous nature.

Domain-specific functional coupling between dorsal and ventral systems during action perception

Visual perception of actions and objects has been shown to activate different cortical systems: action perception system spanning more dorsally, across parietal, frontal, and dorsal temporal regions; object perception relying more strongly the ventral occipitotemporal cortex (VOTC). Compared to the well-established object-domain structure (e.g., faces vs. artifacts) in VOTC, it is less known whether the action perception system is constrained by similar domain principle and whether it communicates with the ventral object recognition system in a domain-specific manner. In a fMRI long-block experiment designed to evaluate both regional activity and task-based functional connectivity (FC) patterns, participants viewed animated videos of a human performing two domains of actions to the same set of meaningless shapes without object-domain information: social-communicative-actions (e.g., waving) and manipulation-actions (e.g., folding). We observed action-domain-specific activations, with the superior temporal sulcus and the right precentral region responding more strongly during social-communicative-action perception; the supramarginal gyrus, inferior and superior parietal lobe, and precentral gyrus during manipulation-action perception. The two domains of action perception systems communicated with VOTC in domain-specific manners: FC between the social-communicative-action system and the bilateral fusiform face area was enhanced during social-communicative-action perception; FC between the manipulation-action system and the left tool-preferring lateral occipitoptemporal cortex was enhanced during manipulation-action perception. There was a significant correlation between the FC-with-action-system and the local activity strength across VOTC voxels. Our findings highlight social- and manipulation-domains of human interaction as an overarching principle of both object and action perception systems, with domain-based functional communication across systems.

Neural bases of social feedback processing and self\u2013other distinction in late childhood: The role of attachment and age

Attachment plays a key role in how children process information about the self and others. Here, we examined the neural bases of interindividual differences in attachment in late childhood and tested whether social cognition-related neural activity varies as function of age. In a small sample of 8-year-old to 12-year-old children (n = 21/19), we used functional magnetic resonance imaging to measure neural responses during social feedback processing and self–other distinction. Attachment was assessed using child self-report. The social feedback processing task presented smiling and angry faces either confirming or disconfirming written information about participant performance on a perceptual game. In addition to observing main effects of facial emotion and performance, an increase in age was related to a shift from negative (i.e., angry faces/bad performance) to positive (i.e., smiling faces/good performance) information processing in the left amygdala/hippocampus, bilateral fusiform face area, bilateral anterior temporal pole (ATP), and left anterior insula. There were no effects of attachment on social feedback processing. The self–other distinction task presented digital morphs between children’s own faces and faces of their mother or stranger females. We observed differential activation in face processing and mentalizing regions in response to self and mother faces versus morphed faces. Furthermore, left ATP activity was associated with attachment anxiety such that greater attachment anxiety was related to a shift from heightened processing of self and mother faces to morphed faces. There were no effects of age on self–other distinction. We discuss our preliminary findings in the context of attachment theory and previous work on social evaluation and self–other processing.

Theta-burst TMS to the posterior superior temporal sulcus decreases resting-state fMRI connectivity across the face processing network.

Humans process faces by using a network of face-selective regions distributed across the brain. Neuropsychological patient studies demonstrate that focal damage to nodes in this network can impair face recognition, but such patients are rare. We approximated the effects of damage to the face network in neurologically normal human participants by using theta burst transcranial magnetic stimulation (TBS). Multi-echo functional magnetic resonance imaging (fMRI) resting-state data were collected pre- and post-TBS delivery over the face-selective right superior temporal sulcus (rpSTS), or a control site in the right motor cortex. Results showed that TBS delivered over the rpSTS reduced resting-state connectivity across the extended face processing network. This connectivity reduction was observed not only between the rpSTS and other face-selective areas, but also between nonstimulated face-selective areas across the ventral, medial, and lateral brain surfaces (e.g., between the right amygdala and bilateral fusiform face areas and occipital face areas). TBS delivered over the motor cortex did not produce significant changes in resting-state connectivity across the face processing network. These results demonstrate that, even without task-induced fMRI signal changes, disrupting a single node in a brain network can decrease the functional connectivity between nodes in that network that have not been directly stimulated.

Self-Regulation of the Fusiform Face Area in Autism Spectrum: A Feasibility Study With Real-Time fMRI Neurofeedback.

One of the most important and early impairments in autism spectrum disorder (ASD) is the abnormal visual processing of human faces. This deficit has been associated with hypoactivation of the fusiform face area (FFA), one of the main hubs of the face-processing network. Neurofeedback based on real-time fMRI (rtfMRI-NF) is a technique that allows the self-regulation of circumscribed brain regions, leading to specific neural modulation and behavioral changes. The aim of the present study was to train participants with ASD to achieve up-regulation of the FFA using rtfMRI-NF, to investigate the neural effects of FFA up-regulation in ASD. For this purpose, three groups of volunteers with normal I.Q. and fluent language were recruited to participate in a rtfMRI-NF protocol of eight training runs in 2 days. Five subjects with ASD participated as part of the experimental group and received contingent feedback to up-regulate bilateral FFA. Two control groups, each one with three participants with typical development (TD), underwent the same protocol: one group with contingent feedback and the other with sham feedback. Whole-brain and functional connectivity analysis using each fusiform gyrus as independent seeds were carried out. The results show that individuals with TD and ASD can achieve FFA up-regulation with contingent feedback. RtfMRI-NF in ASD produced more numerous and stronger short-range connections among brain areas of the ventral visual stream and an absence of the long-range connections to insula and inferior frontal gyrus, as observed in TD subjects. Recruitment of inferior frontal gyrus was observed in both groups during FAA up-regulation. However, insula and caudate nucleus were only recruited in subjects with TD. These results could be explained from a neurodevelopment perspective as a lack of the normal specialization of visual processing areas, and a compensatory mechanism to process visual information of faces. RtfMRI-NF emerges as a potential tool to study visual processing network in ASD, and to explore its clinical potential.

The Human Posterior Superior Temporal Sulcus Samples Visual Space Differently From Other Face-Selective Regions.

Neuroimaging studies show that ventral face-selective regions, including the fusiform face area (FFA) and occipital face area (OFA), preferentially respond to faces presented in the contralateral visual field (VF). In the current study we measured the VF response of the face-selective posterior superior temporal sulcus (pSTS). Across 3 functional magnetic resonance imaging experiments, participants viewed face videos presented in different parts of the VF. Consistent with prior results, we observed a contralateral VF bias in bilateral FFA, right OFA (rOFA), and bilateral human motion-selective area MT+. Intriguingly, this contralateral VF bias was absent in the bilateral pSTS. We then delivered transcranial magnetic stimulation (TMS) over right pSTS (rpSTS) and rOFA, while participants matched facial expressions in both hemifields. TMS delivered over the rpSTS disrupted performance in both hemifields, but TMS delivered over the rOFA disrupted performance in the contralateral hemifield only. These converging results demonstrate that the contralateral bias for faces observed in ventral face-selective areas is absent in the pSTS. This difference in VF response is consistent with face processing models proposing 2 functionally distinct pathways. It further suggests that these models should account for differences in interhemispheric connections between the face-selective areas across these 2 pathways.

The Fusiform Face Area Plays a Greater Role in Holistic Processing for Own-Race Faces Than Other-Race Faces.

Own-race faces are recognized more effectively than other-race faces. This phenomenon is referred to as other-race effect (ORE). Existing behavioral evidence suggests that one of the possible causes of ORE is that own-race faces are processed more holistically than other-race faces. However, little is known about whether such differences in processing also produce distinctive neural responses in the cortical face processing network. To bridge this gap, the present study used fMRI methodology and the composite face paradigm to examine the response patterns of the traditional face-preferential cortical areas (i.e., the bilateral fusiform face areas [FFA] and the bilateral occipital face areas [OFA]) elicited by own-race faces and other-race faces. We found that the right FFA exhibited a neural composite face effect only for own-race faces but not for other-race faces, even with the absence of the race-related difference in behavior composite face effect. These findings suggest that the right FFA plays a greater role in holistic processing of individual own-race faces than other-race faces. They also suggest that the neural composite effect observed in the right FFA is not the exact neural counterpart of the behavioral face composite effect. The findings of the present study revealed that, along the pathway of the bottom-up face processing, own-race faces and other-race faces presented the holistic processing difference as early as when they were processed in the right FFA.

Plastic reorganization of neural systems for perception of others in the congenitally blind

Recent evidence suggests that the function of the core system for face perception might extend beyond visual face-perception to a broader role in person perception. To critically test the broader role of core face-system in person perception, we examined the role of the core system during the perception of others in 7 congenitally blind individuals and 15 sighted subjects by measuring their neural responses using fMRI while they listened to voices and performed identity and emotion recognition tasks. We hypothesised that in people who have had no visual experience of faces, core face-system areas may assume a role in the perception of others via voices. Results showed that emotions conveyed by voices can be decoded in homologues of the core face system only in the blind. Moreover, there was a specific enhancement of response to verbal as compared to non-verbal stimuli in bilateral fusiform face areas and the right posterior superior temporal sulcus showing that the core system also assumes some language-related functions in the blind. These results indicate that, in individuals with no history of visual experience, areas of the core system for face perception may assume a role in aspects of voice perception that are relevant to social cognition and perception of others' emotions.

Mapping structural covariance networks of facial emotion recognition in early psychosis: A pilot study

People with psychosis show deficits recognizing facial emotions and disrupted activation in the underlying neural circuitry. We evaluated associations between facial emotion recognition and cortical thickness using a correlation-based approach to map structural covariance networks across the brain. Fifteen people with an early psychosis provided magnetic resonance scans and completed the Penn Emotion Recognition and Differentiation tasks. Fifteen historical controls provided magnetic resonance scans. Cortical thickness was computed using CIVET and analyzed with linear models. Seed-based structural covariance analysis was done using the mapping anatomical correlations across the cerebral cortex methodology. To map structural covariance networks involved in facial emotion recognition, the right somatosensory cortex and bilateral fusiform face areas were selected as seeds. Statistics were run in SurfStat. Findings showed increased cortical covariance between the right fusiform face region seed and right orbitofrontal cortex in controls than early psychosis subjects. Facial emotion recognition scores were not significantly associated with thickness in any region. A negative effect of Penn Differentiation scores on cortical covariance was seen between the left fusiform face area seed and right superior parietal lobule in early psychosis subjects. Results suggest that facial emotion recognition ability is related to covariance in a temporal-parietal network in early psychosis.

Repetition Suppression and Memory for Faces is Reduced in Adults with Autism Spectrum Conditions.

Autism spectrum conditions (ASC) are associated with a number of atypicalities in face processing, including difficulties in face memory. However, the neural mechanisms underlying this difficulty are unclear. In neurotypical individuals, repeated presentation of the same face is associated with a reduction in activity, known as repetition suppression (RS), in the fusiform face area (FFA). However, to date, no studies have investigated RS to faces in individuals with ASC, or the relationship between RS and face memory. Here, we measured RS to faces and geometric shapes in individuals with a clinical diagnosis of an ASC and in age and IQ matched controls. Relative to controls, the ASC group showed reduced RS to faces in bilateral FFA and reduced performance on a standardized test of face memory. By contrast, RS to shapes in object-selective regions and object memory did not differ between groups. Individual variation in face-memory performance was positively correlated with RS in regions of left parietal and prefrontal cortex. These findings suggest difficulties in face memory in ASC may be a consequence of differences in the way faces are stored and/or maintained across a network of regions involved in both visual perception and short-term/working memory.

The relationship between repetition suppression and face perception.

Repetition of identical face stimuli leads to fMRI response attenuation (fMRI adaptation, fMRIa) in the core face-selective occipito-temporal visual cortical network, involving the bilateral fusiform face area (FFA) and the occipital face area (OFA). However, the functional relevance of fMRIa observed in these regions is unclear as of today. Therefore, here we aimed at investigating the relationship between fMRIa and face perception ability by measuring in the same human participants both the repetition-induced reduction of fMRI responses and identity discrimination performance outside the scanner for upright and inverted face stimuli. In the correlation analysis, the behavioral and fMRI results for the inverted faces were used as covariates to control for the individual differences in overall object perception ability and basic visual feature adaptation processes, respectively. The results revealed a significant positive correlation between the participants' identity discrimination performance and the strength of fMRIa in the core face processing network, but not in the extrastriate body area (EBA). Furthermore, we found a strong correlation of the fMRIa between OFA and FFA and also between OFA and EBA, but not between FFA and EBA. These findings suggest that there is a face-selective component of the repetition-induced reduction of fMRI responses within the core face processing network, which reflects functionally relevant adaptation processes involved in face identity perception.

The functional specialization and collaboration of the bilateral fusiform face areas

The functional specialization and collaboration of the bilateral fusiform face areas

Human brain structure predicts individual differences in preconscious evaluation of facial dominance and trustworthiness.

Social cues conveyed by the human face, such as eye gaze direction, are evaluated even before they are consciously perceived. While there is substantial individual variability in such evaluation, its neural basis is unknown. Here we asked whether individual differences in preconscious evaluation of social face traits were associated with local variability in brain structure. Adult human participants (n = 36) monocularly viewed faces varying in dominance and trustworthiness, which were suppressed from awareness by a dynamic noise pattern shown to the other eye. The time taken for faces to emerge from suppression and become visible (t2e) was used as a measure of potency in competing for visual awareness. Both dominant and untrustworthy faces resulted in slower t2e than neutral faces, with substantial individual variability in these effects. Individual differences in t2e were correlated with gray matter volume in right insula for dominant faces, and with gray matter volume in medial prefrontal cortex, right temporoparietal junction and bilateral fusiform face area for untrustworthy faces. Thus, individual differences in preconscious social processing can be predicted from local brain structure, and separable correlates for facial dominance and untrustworthiness suggest distinct mechanisms of preconscious processing.

P1 and N170 components distinguish human-like and animal-like makeup stimuli

This study used event-related potentials to investigate the sensitivity of P1 and N170 components to human-like and animal-like makeup stimuli, which were derived from pictures of Peking opera characters. As predicted, human-like makeup stimuli elicited larger P1 and N170 amplitudes than did animal-like makeup stimuli. Interestingly, a right hemisphere advantage was observed for human-like but not for animal-like makeup stimuli. Dipole source analyses of 130-200-ms window showed that the bilateral fusiform face area may contribute to the differential sensitivity of the N170 component in response to human-like and animal-like makeup stimuli. The present study suggests that the amplitudes of both the P1 and the N170 are sensitive for the mouth component of face-like stimuli.

Category-specific organization of prefrontal response-facilitation during priming

Perceptual priming is a fundamental long-term memory capability that allows more efficient and faster responding to a stimulus as a result of prior exposure to that stimulus. The two major components of priming are facilitated response expression and improved stimulus identification. Recent fMRI studies have identified a potential neural correlate for response-facilitation, namely the repetition-related activity decrements in prefrontal cortex that are linearly correlated with improvements in reaction times. However, the neural processes underlying such response-facilitation are still unclear. They could be stimulus-selective stimulus-response mapping processes or general response-learning mechanisms. In human imaging studies, behavioral priming has been associated with decreased hemodynamic responses in prefrontal cortex and in category-specific brain regions of the ventral visual stream. Currently, it is unclear whether priming-related response decreases in prefrontal cortex are also category-specific. In this fMRI study, 16 subjects performed a repetition priming task employing category-specific identification judgments on pictures of faces (male/female judgment), scenes (indoor/outdoor judgment) and scrambled ‘noise’ pictures (simple button press). The repeated faces and scenes were identified faster than first presentations indicating priming. Hemodynamic decreases for repetitions were observed in a left inferior (near Brodman Area, BA, 44) and middle frontal (BA8) region of the prefrontal cortex, in category-specific areas of the ventral stream (bilateral fusiform face area, FFA, parahippocampal place area, PPA), and two category-specific right lateral occipital (LOC) regions. Hemodynamic increases for repetitions appeared in the caudate and cerebellum. However, the prefrontal areas were the only regions that showed a correlation between repetition-related reaction time improvement and hemodynamic decrease. Importantly, the correlations were category-specific in their relationship to reaction time improvement: in the left inferior frontal cortex the correlations were specific for scenes whereas and in left middle frontal gyrus they were specific for faces. There were no correlations between behavior and repetition suppression for both LOC regions, FFA and PPA. These data reveal that response-facilitation in prefrontal cortex is organized according to stimulus-properties, compatible with learning of stimulus-response mapping rather than response learning in general.

Recapitulating emotional context: activity of amygdala, hippocampus and fusiform cortex during recollection and familiarity

The amygdala is thought to enhance long-term memory for emotionally arousing events by modulating memory formation and storage in the hippocampus and in neocortical areas. Recent animal studies have raised the possibility that cooperativity between amygdala and hippocampus contributes to the retrieval of fear memories. The functional contributions of the amygdala to the retrieval of emotional memories in humans are less well known. Here, in a functional magnetic resonance imaging experiment, 20 healthy subjects studied neutral words in the context of a fearful or a neutral human face. In a subsequent test, they made 'remember' (conscious recollection of the study context), 'know' (familiarity in the absence of conscious recollection) and 'new' judgements on the studied and newly presented neutral words, in the absence of face stimuli. At test, bilateral amygdala, hippocampus and fusiform face area (FFA) were more strongly activated during recollection than during familiarity. Higher activity for fearful than for neutral study context was found in bilateral FFA during recollection but not during familiarity. This difference recapitulated higher activity for fearful than for neutral context in the FFA during study. These data suggest that the amygdalae and hippocampi contribute to the retrieval of emotion-laden context memories by coordinating the reactivation of stored representations in neocortical areas, such as the FFA. However, there also was a recapitulation of emotional study context in the right amygdala during familiarity only, which might therefore be related to affective implicit memory.