Target visibility and visual awareness modulate amygdala responses to fearful faces

The goals of the present study were twofold. First, we wished to investigate the neural correlates of aware and unaware emotional face perception after characterizing each subject's behavioral performance via signal detection theory methods. Second, we wished to investigate the extent to which amygdala responses to fearful faces depend on the physical characteristics of the stimulus independently of the percept. We show that amygdala responses depend on visual awareness. Under conditions in which subjects were not aware of fearful faces flashed for 33 ms, no differential activation was observed in the amygdala. On the other hand, differential activation was observed for 67 ms fearful targets that the subjects could reliably detect. When trials were divided into hits, misses, correct rejects, and false alarms, we show that target visibility is an important factor in determining amygdala responses to fearful faces. Taken together, our results further challenge the view that amygdala responses occur automatically.     

Unconscious Fearful Priming Followed by a Psychosocial Stress Test Results in Higher Cortisol Levels

Human perception of stress includes an automatic pathway that processes subliminal presented stimuli below the threshold of conscious awareness. Subliminal stimuli can therefore activate the physiologic stress system. Unconscious emotional signals were shown to significantly moderate reactions and responses to subsequent stimuli, an effect called ‘priming’. We hypothesized that subliminal presentation of a fearful signal during the Stroop task compared with an emotionally neutral one will prime stress reactivity in a subsequently applied psychosocial stress task, thereby yielding a significant increase in salivary cortisol. Half of 36 participants were repeatedly presented either a fearful face or a neutral one. After this, all underwent a psychosocial stress task. The fearful group showed a significant increase in cortisol levels (p = 0.022). This change was not affected by sex, age and body mass index, and it also did not change when taking resting cortisol levels into account. Post‐hoc analyses showed that the increase in cortisol in the fearful group started immediately after the psychosocial stress test. Hence, subliminal exposure to a fearful signal in combination with the Stroop and followed by a psychosocial stress test leads to an increase in stress reactivity. Copyright © 2012 John Wiley & Sons, Ltd.     

Context influences early perceptual analysis of faces--an electrophysiological study

Electrophysiological and hemodynamic correlates of processing isolated faces have been investigated extensively over the last decade. A question not addressed thus far is whether the visual scene, which normally surrounds a face or a facial expression, has an influence on how the face is processed. Here we investigated this issue by presenting faces in natural contexts and measuring whether the emotional content of the scene influences processing of a facial expression. Event-related potentials were recorded to faces (fearful/neutral) embedded in scene contexts (fearful/neutral) while participants performed an orientation-decision task (face upright or inverted). Two additional experiments were run, one to examine the effects of context that occur without a face and the other to evaluate the effects of faces isolated from contexts. Faces without any context showed the largest N170 amplitudes. The presence of a face in a fearful context enhances the N170 amplitude over a face in neutral contexts, an effect that is strongest for fearful faces on left occipito-temporal sites. This N170 effect, and the corresponding topographic distribution, was not found for contexts-only, indicating that the increased N170 amplitude results from the combination of face and fearful context. These findings suggest that the context in which a face appears may influence how it is encoded.     

Cognitive coping style modulates neural responses to emotional faces in healthy humans: a 3-T FMRI study

Repression designates coping strategies that aim to shield the organism from distressing stimuli by disregarding their aversive characteristics. In contrast, sensitization comprises coping strategies that are employed to reduce situational uncertainty such as analyzing the environment. Functional magnetic resonance imaging was used to study neural correlates of coping styles during the perception of threatening and nonthreatening socially relevant information. Pictures of human faces bearing fearful (ambiguously threatening), angry (unambiguously threatening), happy (nonthreatening), and neutral expressions were presented masked and unmasked. Two groups of subjects were examined who were defined as consistent repressors versus consistent sensitizers with the Mainz Coping Inventory. Sensitizers tended to exhibit stronger neural responses in the amygdala to unmasked fearful faces compared with repressors. Overall, repressors were cortically more responsive to fearful (ambiguously threatening) and happy (nonthreatening) facial expressions than sensitizers, whereas sensitizers presented an enhanced responsivity to angry faces in several prefrontal areas, that is, unambiguously threatening expressions. Results from time series analyses suggest that sensitizers could exhibit less top-down cortical regulation of the amygdala than repressors in the processing of fearful faces. An increased responsivity of the amygdala to ambiguously threatening stimuli may represent a biological determinant of sensitizers' feelings of uncertainty.     

Activity in face-responsive brain regions is modulated by invisible, attended faces: evidence from masked priming

It is often assumed that neural activity in face-responsive regions of primate cortex correlates with conscious perception of faces. However, whether such activity occurs without awareness is still debated. Using functional magnetic resonance imaging (fMRI) in conjunction with a novel masked face priming paradigm, we observed neural modulations that could not be attributed to perceptual awareness. More specifically, we found reduced activity in several classic face-processing regions, including the "fusiform face area," "occipital face area," and superior temporal sulcus, when a face was preceded by a briefly flashed image of the same face, relative to a different face, even when 2 images of the same face differed. Importantly, unlike most previous studies, which have minimized awareness by using conditions of inattention, the present results occurred when the stimuli (the primes) were attended. By contrast, when primes were perceived consciously, in a long-lag priming paradigm, we found repetition-related activity increases in additional frontal and parietal regions. These data not only demonstrate that fMRI activity in face-responsive regions can be modulated independently of perceptual awareness, but also document where such subliminal face-processing occurs (i.e., restricted to face-responsive regions of occipital and temporal cortex) and to what extent (i.e., independent of the specific image).     

Dynamic perception of facial affect and identity in the human brain

Functional magnetic resonance imaging (fMRI) was used to compare brain activation to static facial displays versus dynamic changes in facial identity or emotional expression. Static images depicted prototypical fearful, angry and neutral expressions. Identity morphs depicted identity changes from one person to another, always with neutral expressions. Emotion morphs depicted expression changes from neutral to fear or anger, creating the illusion that the actor was 'getting scared' or 'getting angry' in real-time. Brain regions implicated in processing facial affect, including the amygdala and fusiform gyrus, showed greater responses to dynamic versus static emotional expressions, especially for fear. Identity morphs activated a dorsal fronto-cingulo-parietal circuit and additional ventral areas, including the amygdala, that also responded to the emotion morphs. Activity in the superior temporal sulcus discriminated emotion morphs from identity morphs, extending its known role in processing biologically relevant motion. The results highlight the importance of temporal cues in the neural coding of facial displays.     

Similar frontal and distinct posterior cortical regions mediate visual and auditory perceptual awareness

Activity in ventral visual cortex is a consistent neural correlate of visual consciousness. However, activity in this area seems insufficient to produce awareness without additional involvement of frontoparietal regions. To test the generality of the frontoparietal response, neural correlates of auditory awareness were investigated in a paradigm that previously has revealed frontoparietal activity during conscious visual perception. A within-experiment comparison showed that frontal regions were related to both visual and auditory awareness, whereas parietal activity was correlated with visual awareness and superior temporal activity with auditory awareness. These results indicate that frontal regions interact with specific posterior regions to produce awareness in different sensory modalities.     

Enhanced processing of threat stimuli under limited attentional resources

The ability to process stimuli that convey potential threat, under conditions of limited attentional resources, confers adaptive advantages. This study examined the neurobiology underpinnings of this capacity. Employing an attentional blink paradigm, in conjunction with functional magnetic resonance imaging, we manipulated the salience of the second of 2 face target stimuli (T2), by varying emotionality. Behaviorally, fearful T2 faces were identified significantly more than neutral faces. Activity in fusiform face area increased with correct identification of T2 faces. Enhanced activity in rostral anterior cingulate cortex (rACC) accounted for the benefit in detection of fearful stimuli reflected in a significant interaction between target valence and correct identification. Thus, under conditions of limited attention resources activation in rACC correlated with enhanced processing of emotional stimuli. We suggest that these data support a model in which a prefrontal "gate" mechanism controls conscious access of emotional information under conditions of limited attentional resources.     

The modular neuroarchitecture of social judgments on faces

Face-derived information on trustworthiness and attractiveness crucially influences social interaction. It is, however, unclear to what degree the functional neuroanatomy of these complex social judgments on faces reflects genuine social versus basic emotional and cognitive processing. To disentangle social from nonsocial contributions, we assessed commonalities and differences between the functional networks activated by judging social (trustworthiness, attractiveness), emotional (happiness), and cognitive (age) facial traits. Relative to happiness and age evaluations, both trustworthiness and attractiveness judgments selectively activated the dorsomedial prefrontal cortex and inferior frontal gyrus, forming a core social cognition network. Moreover, they also elicited a higher amygdalar response than even the emotional control condition. Both social judgments differed, however, in their top-down modulation of face-sensitive regions: trustworthiness judgments recruited the posterior superior temporal sulcus, whereas attractiveness judgments recruited the fusiform gyrus. Social and emotional judgments converged and, therefore, likely interact in the ventromedial prefrontal cortex. Social and age judgments, on the other hand, commonly engaged the anterior insula, inferior parietal cortex, and dorsolateral prefrontal cortex, which appear to subserve more cognitive aspects in social evaluation. These findings demonstrate the modularity of social judgments on human faces by separating the neural correlates of social, face-specific, emotional, and cognitive processing facets.     

Cerebral bases of subliminal and supraliminal priming during reading

Several studies have investigated the neural correlates of conscious perception by contrasting functional magnetic resonance imaging (fMRI) activation to conscious and nonconscious visual stimuli. The results often reveal an amplification of posterior occipito-temporal activation and its extension into a parieto-frontal network. However, some of these effects might be due to a greater deployment of attentional or strategical processes in the conscious condition. Here, we examined the brain activity evoked by visible and invisible stimuli, both of which were irrelevant to the task. We collected fMRI data in a masking paradigm in which subliminal versus supraliminal letter strings were presented as primes while subjects focused attention on another subsequent, highly visible target word. Under those conditions, prime visibility was associated with greater activity confined to bilateral posterior occipito-temporal cortices, without extension into frontal and parietal cortices. However, supraliminal primes, compared with subliminal primes, evoked more extensive repetition suppression in a widely distributed set of parieto-frontal areas. Furthermore, only supraliminal primes caused phonological repetition enhancement in left inferior frontal and anterior insular cortex. Those results suggest a 2-stage view of conscious access: Relative to masked stimuli, unmasked stimuli elicit increased occipito-temporal activity, thus allowing them to compete for global conscious access and to induce priming in multiple distant areas. In the absence of attention, however, their access to a second stage of distributed parieto-frontal processing may remain blocked.     

Changes in connectivity profiles as a mechanism for strategic control over interfering subliminal information

Human behavior can be influenced by information that is not consciously perceived. Recent behavioral and electrophysiological evidence suggests, however, that the processing of subliminal stimuli is not completely beyond an observer's conscious control. The present study aimed to characterize the cortical network that implements strategic control over interfering subliminal information at multiple stages. Fourteen participants underwent functional magnetic resonance imaging (fMRI) scanning while performing a metacontrast masking paradigm. We systematically varied the amount of conflicting versus non-conflicting trials across experimental blocks, and behavioral performance demonstrated strategic effects whenever a high proportion of subliminal prime stimuli induced response competition. A psychophysiological interaction analysis revealed the pre-supplementary motor area (pre-SMA) to exhibit context-dependent covariation with activation in the lateral occipital complex (LOC) and the putamen. The pre-SMA thereby appears to fulfill a superordinate function in the control of processing subliminal information by simultaneously modulating perceptual analysis and motor selection.     

Electrophysiological correlates of rapid spatial orienting towards fearful faces

We investigated the spatio-temporal dynamic of attentional bias towards fearful faces. Twelve participants performed a covert spatial orienting task while recording visual event-related brain potentials (VEPs). Each trial consisted of a pair of faces (one emotional and one neutral) briefly presented in the upper visual field, followed by a unilateral bar presented at the location of one of the faces. Participants had to judge the orientation of the bar. Comparing VEPs to bars shown at the location of an emotional (valid) versus neutral (invalid) face revealed an early effect of spatial validity: the lateral occipital P1 component (approximately 130 ms post-stimulus) was selectively increased when a bar replaced a fearful face compared to when the same bar replaced a neutral face. This effect was not found with upright happy faces or inverted fearful faces. A similar amplification of P1 has previously been observed in electrophysiological studies of spatial attention using non-emotional cues. In a behavioural control experiment, participants were also better at discriminating the orientation of the bar when it replaced a fearful rather than a neutral face. In addition, VEPs time-locked to the face-pair onset revealed a C1 component (approximately 90 ms) that was greater for fearful than happy faces. Source localization (LORETA) confirmed an extrastriate origin of the P1 response showing a spatial validity effect, and a striate origin of the C1 response showing an emotional valence effect. These data suggest that activity in primary visual cortex might be enhanced by fear cues as early as 90 ms post-stimulus, and that such effects might result in a subsequent facilitation of sensory processing for a stimulus appearing at the same location. These results provide evidence for neural mechanisms allowing rapid, exogenous spatial orienting of attention towards fear stimuli.     

Controlling emotional expression: behavioral and neural correlates of nonimitative emotional responses

Emotional facial expressions can engender similar expressions in others. However, adaptive social and motivational behavior can require individuals to suppress, conceal, or override prepotent imitative responses. We predicted, in line with a theory of "emotion contagion," that when viewing a facial expression, expressing a different emotion would manifest as behavioral conflict and interference. We employed facial electromyography (EMG) and functional magnetic resonance imaging (fMRI) to investigate brain activity related to this emotion expression interference (EEI) effect, where the expressed response was either concordant or discordant with the observed emotion. The Simon task was included as a nonemotional comparison for the fMRI study. Facilitation and interference effects were observed in the latency of facial EMG responses. Neuroimaging revealed activation of distributed brain regions including anterior right inferior frontal gyrus (brain area [BA] 47), supplementary motor area (facial area), posterior superior temporal sulcus (STS), and right anterior insula during emotion expression-associated interference. In contrast, nonemotional response conflict (Simon task) engaged a distinct frontostriatal network. Individual differences in empathy and emotion regulatory tendency predicted the magnitude of EEI-evoked regional activity with BA 47 and STS. Our findings point to these regions as providing a putative neural substrate underpinning a crucial adaptive aspect of social/emotional behavior.     

Functional neuronal processing of body odors differs from that of similar common odors

Visual and auditory stimuli of high social and ecological importance are processed in the brain by specialized neuronal networks. To date, this has not been demonstrated for olfactory stimuli. By means of positron emission tomography, we sought to elucidate the neuronal substrates behind body odor perception to answer the question of whether the central processing of body odors differs from perceptually similar nonbody odors. Body odors were processed by a network that was distinctly separate from common odors, indicating a separation in the processing of odors based on their source. Smelling a friend's body odor activated regions previously seen for familiar stimuli, whereas smelling a stranger activated amygdala and insular regions akin to what has previously been demonstrated for fearful stimuli. The results provide evidence that social olfactory stimuli of high ecological relevance are processed by specialized neuronal networks similar to what has previously been demonstrated for auditory and visual stimuli.     

Cognitive response profile of the human fusiform face area as determined by MEG

Activation in or near the fusiform gyrus was estimated to faces and control stimuli. Activation peaked at 165 ms and was strongest to digitized photographs of human faces, regardless of whether they were presented in color or grayscale, suggesting that face- and color-specific areas are functionally separate. Schematic sketche evoked approximately 30% less activation than did face photographs. Scrambling the locations of facial features reduced the response by approximately 25% in either hemisphere, suggesting that configurational versus analytic processing is not lateralized at this latency. Animal faces evoked approximately 50% less activity, and common objects, animal bodies or sensory controls evoked approximately 80% less activity than human faces. The (small) responses evoked by meaningless control images were stronger when they included surfaces and shading, suggesting that the fusiform gyrus may use these features in constructing its face-specific response. Putative fusiform activation was not significantly related to stimulus repetition, gender or emotional expression. A midline occipital source significantly distinguished between faces and control images as early as 110 ms, but was more sensitive to sensory qualities. This source significantly distinguished happy and sad faces from those with neutral expressions. We conclude that the fusiform gyrus may selectively encode faces at 165 ms, transforming sensory input for further processing.     

Altered electrodermal response to facial expression after closed head injury

Summary : The objective was to determine whether diffuse damage to orbital and ventromedial regions of the prefrontal cortex usually associated with moderate-to-severe closed head injury (CHI) would affect the ability to perceive and respond to socially relevant information.

Methods : Participants with CHI and age-matched non-injured controls were presented with faces that varied with respect to emotional expression while electrodermal activity (EDA) was monitored. Cognitive and general adaptive functioning was also assessed.

Results : CHI was associated with a failure to increase EDA in response to negative facial expressions and with reduced ability to identify negative expressions, especially fear. The groups differed on other signs of orbital/medial prefrontal damage such as anosmia and in general social adaptability and awareness-of-deficit as measured by the Brock Adaptive Functioning Questionnaire.

Conclusions : CHI affected the ability to identify and respond to negative facial expression. Addressing these deficits may enhance rehabilitative efforts within the social domain.     

Emotional context enhances auditory novelty processing in superior temporal gyrus

Visualizing emotionally loaded pictures intensifies peripheral reflexes toward sudden auditory stimuli, suggesting that the emotional context may potentiate responses elicited by novel events in the acoustic environment. However, psychophysiological results have reported that attentional resources available to sounds become depleted, as attention allocation to emotional pictures increases. These findings have raised the challenging question of whether an emotional context actually enhances or attenuates auditory novelty processing at a central level in the brain. To solve this issue, we used functional magnetic resonance imaging to first identify brain activations induced by novel sounds (NOV) when participants made a color decision on visual stimuli containing both negative (NEG) and neutral (NEU) facial expressions. We then measured modulation of these auditory responses by the emotional load of the task. Contrary to what was assumed, activation induced by NOV in superior temporal gyrus (STG) was enhanced when subjects responded to faces with a NEG emotional expression compared with NEU ones. Accordingly, NOV yielded stronger behavioral disruption on subjects' performance in the NEG context. These results demonstrate that the emotional context modulates the excitability of auditory and possibly multimodal novelty cerebral regions, enhancing acoustic novelty processing in a potentially harming environment.     

Endogenous testosterone modulates prefrontal-amygdala connectivity during social emotional behavior

It is clear that the steroid hormone testosterone plays an important role in the regulation of social emotional behavior, but it remains unknown which neural circuits mediate these hormonal influences in humans. We investigated the modulatory effects of endogenous testosterone on the control of social emotional behavior by applying functional magnetic resonance imaging while healthy male participants performed a social approach-avoidance task. This task operationalized social emotional behavior by having participants approach and avoid emotional faces by pulling and pushing a joystick, respectively. Affect-congruent trials mapped the automatic tendency to approach happy faces and avoid angry faces. Affect-incongruent trials required participants to override those automatic action tendencies and select the opposite response (approach-angry, avoid-happy). The social emotional control required by affect-incongruent responses resulted in longer reaction times (RTs) and increased activity at the border of the ventrolateral prefrontal cortex and frontal pole (VLPFC/FP). We show that endogenous testosterone modulates these cerebral congruency effects through 2 mechanisms. First, participants with lower testosterone levels generate larger VLPFC/FP responses during affect-incongruent trials. Second, during the same trials, endogenous testosterone modulates the effective connectivity between the VLPFC/FP and the amygdala. These results indicate that endogenous testosterone influences local prefrontal activity and interregional connectivity supporting the control of social emotional behavior.     

The link between facial feedback and neural activity within central circuitries of emotion--new insights from botulinum toxin-induced denervation of frown muscles

Afferent feedback from muscles and skin has been suggested to influence our emotions during the control of facial expressions. Recent imaging studies have shown that imitation of facial expressions is associated with activation in limbic regions such as the amygdala. Yet, the physiological interaction between this limbic activation and facial feedback remains unclear. To study if facial feedback effects on limbic brain responses during intentional imitation of facial expressions, we applied botulinum toxin (BTX)-induced denervation of frown muscles in combination with functional magnetic resonance imaging as a reversible lesion model to minimize the occurrence of afferent muscular and cutaneous input. We show that, during imitation of angry facial expressions, reduced feedback due to BTX treatment attenuates activation of the left amygdala and its functional coupling with brain stem regions implicated in autonomic manifestations of emotional states. These findings demonstrate that facial feedback modulates neural activity within central circuitries of emotion during intentional imitation of facial expressions. Given that people tend to mimic the emotional expressions of others, this could provide a potential physiological basis for the social transfer of emotion.     

Mimetic muscles and emotions: Hans Memling's fifteenth century masterpiece, "Last judgment," as a study for aesthetic surgery

As the most recognizable part of the body, the face has always interested, not only artists, but doctors as well. Each has had their own perception of facial beauty. The task for plastic and aesthetic surgery regarding the face is to reconstruct, not only traumatic lesions, but also to prevent the effects of facial tissue aging. It is also important to preserve the aesthetic values of the face in different emotional conditions. Those conditions are partially represented by mimetic or facial muscles. One might suggest that the perception of human beings portrayed by the artists could be very helpful in the realm of plastic and aesthetic surgery. Take, for example, Hans Memling, a fifthteenth century Flemish artist whose masterpiece ``Last Judgment' is exhibited at Gdańsk National Museum in Poland. The fortunate individuals on the left side of the painting are queuing at heaven's gate to receive their reward. Their faces are smooth with smiles, displaying blessings and happiness. The right-hand side of the painting exemplifies the expression of fear and the drama of the situation. These sinners have been damned and sentenced to hell by evil creatures. The fear, pain, and tragedy of condemnation fill their faces. For plastic and cosmetic surgeons, studying the works of great artists has not been as valuable as using the emotionless and intangible figures of an anatomy book. Undoubtedly, the only useful paintings and sculptures are those that are full of expression with the face displaying a plethora of emotions. In all surgical approaches where mimetic muscles are concerned, one has to remember and be conscious of the fact that the face is a very significant part of our body.