Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect

This study examined whether differential neural responses are evoked by emotional stimuli with and without conscious perception, in a patient with visual neglect and extinction. Stimuli were briefly shown in either right, left, or both fields during event-related fMRI. On bilateral trials, either a fearful or neutral left face appeared with a right house, and it could either be extinguished from awareness or perceived. Seen faces in left visual field (LVF) activated primary visual cortex in the damaged right-hemisphere and bilateral fusiform gyri. Extinguished left faces increased activity in striate and extrastriate cortex, compared with right houses only. Critically, fearful faces activated the left amygdala and extrastriate cortex both when seen and when extinguished; as well as bilateral orbitofrontal and intact right superior parietal areas. Comparison of perceived versus extinguished faces revealed no difference in amygdala for fearful faces. Conscious perception increased activity in fusiform, parietal and prefrontal areas of the left-hemisphere, irrespective of emotional expression; while a differential emotional response to fearful faces occurring specifically with awareness was found in bilateral parietal, temporal, and frontal areas. These results demonstrate that amygdala and orbitofrontal cortex can be activated by emotional stimuli even without awareness after parietal damage; and that substantial unconscious residual processing can occur within spared brain areas well beyond visual cortex, despite neglect and extinction.     

Backward masked fearful faces enhance contralateral occipital cortical activity for visual targets within the spotlight of attention

Spatial attention has been argued to be adaptive by enhancing the processing of visual stimuli within the ‘spotlight of attention’. We previously reported that crude threat cues (backward masked fearful faces) facilitate spatial attention through a network of brain regions consisting of the amygdala, anterior cingulate and contralateral visual cortex. However, results from previous functional magnetic resonance imaging (fMRI) dot-probe studies have been inconclusive regarding a fearful face-elicited contralateral modulation of visual targets. Here, we tested the hypothesis that the capture of spatial attention by crude threat cues would facilitate processing of subsequently presented visual stimuli within the masked fearful face-elicited ‘spotlight of attention’ in the contralateral visual cortex. Participants performed a backward masked fearful face dot-probe task while brain activity was measured with fMRI. Masked fearful face left visual field trials enhanced activity for spatially congruent targets in the right superior occipital gyrus, fusiform gyrus and lateral occipital complex, while masked fearful face right visual field trials enhanced activity in the left middle occipital gyrus. These data indicate that crude threat elicited spatial attention enhances the processing of subsequent visual stimuli in contralateral occipital cortex, which may occur by lowering neural activation thresholds in this retinotopic location.     

Functional plasticity in ventral temporal cortex following cognitive rehabilitation of a congenital prosopagnosic

We used functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) to measure neural changes associated with training configural processing in congenital prosopagnosia, a condition in which face identification abilities are not properly developed in the absence of brain injury or visual problems. We designed a task that required discriminating faces by their spatial configuration and, after extensive training, prosopagnosic MZ significantly improved at face identification. Event-related potential results revealed that although the N170 was not selective for faces before training, its selectivity after training was normal. fMRI demonstrated increased functional connectivity between ventral occipital temporal face-selective regions (right occipital face area and right fusiform face area) that accompanied improvement in face recognition. Several other regions showed fMRI activity changes with training; the majority of these regions increased connectivity with face-selective regions. Together, the neural mechanisms associated with face recognition improvements involved strengthening early face-selective mechanisms and increased coordination between face-selective and nonselective regions, particularly in the right hemisphere.     

Affective learning modulates spatial competition during low-load attentional conditions

It has been hypothesized that the amygdala mediates the processing advantage of emotional items. In the present study, we employed functional magnetic resonance imaging (fMRI) to investigate how fear conditioning affected the visual processing of task-irrelevant faces. We hypothesized that faces previously paired with shock (threat faces) would more effectively vie for processing resources during conditions involving spatial competition. To investigate this question, following conditioning, participants performed a letter-detection task on an array of letters that was superimposed on task-irrelevant faces. Attentional resources were manipulated by having participants perform an easy or a difficult search task. Our findings revealed that threat fearful faces evoked stronger responses in the amygdala and fusiform gyrus relative to safe fearful faces during low-load attentional conditions, but not during high-load conditions. Consistent with the increased processing of shock-paired stimuli during the low-load condition, such stimuli exhibited increased behavioral priming and fMRI repetition effects relative to unpaired faces during a subsequent implicit-memory task. Overall, our results suggest a competition model in which affective significance signals from the amygdala may constitute a key modulatory factor determining the neural fate of visual stimuli. In addition, it appears that such competitive advantage is only evident when sufficient processing resources are available to process the affective stimulus.     

5‐HTTLPR differentially predicts brain network responses to emotional faces

The effects of the 5‐HTTLPR polymorphism on neural responses to emotionally salient faces have been studied extensively, focusing on amygdala reactivity and amygdala‐prefrontal interactions. Despite compelling evidence that emotional face paradigms engage a distributed network of brain regions involved in emotion, cognitive and visual processing, less is known about 5‐HTTLPR effects on broader network responses. To address this, we evaluated 5‐HTTLPR differences in the whole‐brain response to an emotional faces paradigm including neutral, angry and fearful faces using functional magnetic resonance imaging in 76 healthy adults. We observed robust increased response to emotional faces in the amygdala, hippocampus, caudate, fusiform gyrus, superior temporal sulcus and lateral prefrontal and occipito‐parietal cortices. We observed dissociation between 5‐HTTLPR groups such that L_AL_A individuals had increased response to only angry faces, relative to neutral ones, but S′ carriers had increased activity for both angry and fearful faces relative to neutral. Additionally, the response to angry faces was significantly greater in L_AL_A individuals compared to S′ carriers and the response to fearful faces was significantly greater in S′ carriers compared to L_AL_A individuals. These findings provide novel evidence for emotion‐specific 5‐HTTLPR effects on the response of a distributed set of brain regions including areas responsive to emotionally salient stimuli and critical components of the face‐processing network. These findings provide additional insight into neurobiological mechanisms through which 5‐HTTLPR genotype may affect personality and related risk for neuropsychiatric illness. Hum Brain Mapp 36:2842–2851, 2015. © 2015 Wiley Periodicals, Inc.     

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.     

Impact of voice on emotional judgment of faces: an event-related fMRI study

Emotional information can be conveyed by various means of communication, such as propositional content, speech intonation, facial expression, and gestures. Prior studies have demonstrated that inputs from one modality can alter perception in another modality. To evaluate the impact of emotional intonation on ratings of emotional faces, a behavioral study first was carried out. Second, functional magnetic resonance (fMRI) was used to identify brain regions that mediate crossmodal effects of emotional prosody on judgments of facial expressions. In the behavioral study, subjects rated fearful and neutral facial expressions as being more fearful when accompanied by a fearful voice as compared to the same facial expressions without concomitant auditory stimulus, whereas no such influence on rating of faces was found for happy voices. In the fMRI experiment, this shift in rating of facial expressions in presence of a fearfully spoken sentence was correlated with the hemodynamic response in the left amygdala extending into the periamygdaloid cortex, which suggests that crossmodal effects on cognitive judgments of emotional information are mediated via these neuronal structures. Furthermore, significantly stronger activations were found in the mid-portion of the right fusiform gyrus during judgment of facial expressions in presence of fearful as compared to happy intonations, indicating that enhanced processing of faces within this region can be induced by the presence of threat-related information perceived via the auditory modality. Presumably, these increased extrastriate activations correspond to enhanced alertness, whereas responses within the left amygdala modulate cognitive evaluation of emotional facial expressions.     

Neural substrates of facial emotion processing using fMRI

We identified human brain regions involved in the perception of sad, frightened, happy, angry, and neutral facial expressions using functional magnetic resonance imaging (fMRI). Twenty-one healthy right-handed adult volunteers (11 men, 10 women; aged 18-45; mean age 21.6 years) participated in four separate runs, one for each of the four emotions. Participants viewed blocks of emotionally expressive faces alternating with blocks of neutral faces and scrambled images. In comparison with scrambled images, neutral faces activated the fusiform gyri, the right lateral occipital gyrus, the right superior temporal sulcus, the inferior frontal gyri, and the amygdala/entorhinal cortex. In comparisons of emotional and neutral faces, we found that (1) emotional faces elicit increased activation in a subset of cortical regions involved in neutral face processing and in areas not activated by neutral faces; (2) differences in activation as a function of emotion category were most evident in the frontal lobes; (3) men showed a differential neural response depending upon the emotion expressed but women did not.     

The representation of parts and wholes in face-selective cortex

Although face perception is often characterized as depending on holistic, rather than part-based, processing, there is behavioral evidence for independent representations of face parts. Recent work has linked "face-selective" regions defined with functional magnetic resonance imaging (fMRI) to holistic processing, but the response of these areas to face parts remains unclear. Here we examine part-based versus holistic processing in "face-selective" visual areas using face stimuli manipulated in binocular disparity to appear either behind or in front of a set of stripes [Nakayama, K., Shimojo, S., & Silverman, G. H. Stereoscopic depth: Its relation to image segmentation, grouping, and the recognition of occluded objects. Perception, 18, 55-68, 1989]. While the first case will be "filled in" by the visual system and perceived holistically, we demonstrate behaviorally that the latter cannot be completed amodally, and thus is perceived as parts. Using these stimuli in fMRI, we found significant responses to both depth manipulations in inferior occipital gyrus and middle fusiform gyrus (MFG) "face-selective" regions, suggesting that neural populations in these areas encode both parts and wholes. In comparison, applying these depth manipulations to control stimuli (alphanumeric characters) elicited much smaller signal changes within face-selective regions, indicating that the part-based representation for faces is separate from that for objects. The combined adaptation data also showed an interaction of depth and familiarity within the right MFG, with greater adaptation in the back (holistic) condition relative to parts for familiar but not unfamiliar faces. Together, these data indicate that face-selective regions of occipito-temporal cortex engage in both part-based and holistic processing. The relative recruitment of such representations may be additionally influenced by external factors such as familiarity.     

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.