Stimulus arousal drives amygdalar responses to emotional expressions across sensory modalities.

The factors that drive amygdalar responses to emotionally significant stimuli are still a matter of debate - particularly the proneness of the amygdala to respond to negatively-valenced stimuli has been discussed controversially. Furthermore, it is uncertain whether the amygdala responds in a modality-general fashion or whether modality-specific idiosyncrasies exist. Therefore, the present functional magnetic resonance imaging (fMRI) study systematically investigated amygdalar responding to stimulus valence and arousal of emotional expressions across visual and auditory modalities. During scanning, participants performed a gender judgment task while prosodic and facial emotional expressions were presented. The stimuli varied in stimulus valence and arousal by including neutral, happy and angry expressions of high and low emotional intensity. Results demonstrate amygdalar activation as a function of stimulus arousal and accordingly associated emotional intensity regardless of stimulus valence. Furthermore, arousal-driven amygdalar responding did not depend on the visual and auditory modalities of emotional expressions. Thus, the current results are consistent with the notion that the amygdala codes general stimulus relevance across visual and auditory modalities irrespective of valence. In addition, whole brain analyses revealed that effects in visual and auditory areas were driven mainly by high intense emotional facial and vocal stimuli, respectively, suggesting modality-specific representations of emotional expressions in auditory and visual cortices.

Early brain responses to affective faces: A simultaneous EEG-fMRI study.

The spatio-temporal neural basis of earliest differentiation between emotional and neutral facial expressions is a matter of debate. The present study used concurrent electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) in order to investigate the 'when' and 'where' of earliest prioritization of emotional over neutral expressions. We measured event-related potentials (ERPs) and blood oxygen dependent (BOLD) signal changes in response to facial expressions of varying emotional intensity and different valence categories. Facial expressions were presented superimposed by two horizontal bars and participants engaged in a focal bars task (low load, high load), in order to manipulate the availability of attentional resources during face perception. EEG data revealed the earliest expression effects in the P1 range (76-128 ms) as a parametric function of stimulus arousal independent of load conditions. Conventional fMRI data analysis also demonstrated significant modulations as a function of stimulus arousal, independent of load, in amygdala, superior temporal sulcus, fusiform gyrus and lateral occipital cortex. Correspondingly, EEG-informed fMRI analysis revealed a significant positive correlation between single-trial P1 amplitudes and BOLD responses in amygdala and lateral posterior occipital cortex. Our results are in line with the hypothesis of the amygdala as fast responding relevance detector and corresponding effects in early visual face processing areas across facial expressions and load conditions.

Loud and angry: sound intensity modulates amygdala activation to angry voices in social anxiety disorder.

Angry expressions of both voices and faces represent disorder-relevant stimuli in social anxiety disorder (SAD). Although individuals with SAD show greater amygdala activation to angry faces, previous work has failed to find comparable effects for angry voices. Here, we investigated whether voice sound-intensity, a modulator of a voice's threat-relevance, affects brain responses to angry prosody in SAD. We used event-related functional magnetic resonance imaging to explore brain responses to voices varying in sound intensity and emotional prosody in SAD patients and healthy controls (HCs). Angry and neutral voices were presented either with normal or high sound amplitude, while participants had to decide upon the speaker's gender. Loud vs normal voices induced greater insula activation, and angry vs neutral prosody greater orbitofrontal cortex activation in SAD as compared with HC subjects. Importantly, an interaction of sound intensity, prosody and group was found in the insula and the amygdala. In particular, the amygdala showed greater activation to loud angry voices in SAD as compared with HC subjects. This finding demonstrates a modulating role of voice sound-intensity on amygdalar hyperresponsivity to angry prosody in SAD and suggests that abnormal processing of interpersonal threat signals in amygdala extends beyond facial expressions in SAD.

Effects of emotional intensity under perceptual load: An event-related potentials (ERPs) study.

Effects of emotional intensity and valence on visual event-related potentials (ERPs) are still poorly understood, in particular in the context of limited attentional resources. In the present EEG study, we investigated the effect of emotional intensity of different emotional facial expressions on P1, N170, early posterior negativity (EPN) and late positive potential (LPP) while varying the amount of available attentional resources. A new stimulus set comprising 90 full color pictures of neutral, happy (low, high intensity), and angry (low, high intensity) expressions was developed. These facial expressions were presented centrally, superimposed by two horizontal bars, and participants engaged in a focal bars task. Availability of attentional resources was varied in two conditions by manipulating the difficulty of the focal bars task (low vs. high perceptual load). Our findings demonstrate intensity and valence effects of task-irrelevant facial expressions on early (N170) and intermediate processing stages (EPN). In addition, task-related effects of perceptual load evolved at intermediate processing stages and were full blown in the time window of LPP. In line with limited resource accounts, valence effects on N170 and EPN were reduced under high perceptual load. Interestingly, apart from this valence by load interaction no further interactions between stimulus and task-driven factors were obtained: Effects of emotional intensity were not modulated by the perceptual load of the focal bars task, indicating that emotional intensity was processed even though attentional resources were heavily restricted.

Neural basis of processing threatening voices in a crowded auditory world.

In real world situations, we typically listen to voice prosody against a background crowded with auditory stimuli. Voices and background can both contain behaviorally relevant features and both can be selectively in the focus of attention. Adequate responses to threat-related voices under such conditions require that the brain unmixes reciprocally masked features depending on variable cognitive resources. It is unknown which brain systems instantiate the extraction of behaviorally relevant prosodic features under varying combinations of prosody valence, auditory background complexity and attentional focus. Here, we used event-related functional magnetic resonance imaging to investigate the effects of high background sound complexity and attentional focus on brain activation to angry and neutral prosody in humans. Results show that prosody effects in mid superior temporal cortex were gated by background complexity but not attention, while prosody effects in the amygdala and anterior superior temporal cortex were gated by attention but not background complexity, suggesting distinct emotional prosody processing limitations in different regions. Crucially, if attention was focused on the highly complex background, the differential processing of emotional prosody was prevented in all brain regions, suggesting that in a distracting, complex auditory world even threatening voices may go unnoticed.

Effects of Intensity of Facial Expressions on Amygdalar Activation Independently of Valence.

For several stimulus categories (e.g., pictures, odors, and words), the arousal of both negative and positive stimuli has been shown to modulate amygdalar activation. In contrast, previous studies did not observe similar amygdalar effects in response to negative and positive facial expressions with varying intensity of facial expressions. Reasons for this discrepancy may be related to analytical strategies, experimental design and stimuli. Therefore, the present study aimed at re-investigating whether the intensity of facial expressions modulates amygdalar activation by circumventing limitations of previous research. Event-related functional magnetic resonance imaging was used to assess brain activation while participants observed a static neutral expression and positive (happy) and negative (angry) expressions of either high or low intensity from an ecologically valid, novel stimulus set. The ratings of arousal and intensity were highly correlated. We found that amygdalar activation followed a u-shaped activation pattern with highest activation to high intense facial expressions as compared to low intensity facial expressions and to the neutral expression irrespective of valence, suggesting a critical role of the amygdala in valence-independent arousal processing of facial expressions. Additionally, consistent with previous studies, intensity effects were also found in visual areas and generally increased activation to angry versus happy faces were found in visual cortex and insula, indicating enhanced visual representations of high arousing facial expressions and increased visual and somatosensory representations of threat.

Brain activation to briefly presented emotional words: effects of stimulus awareness.

It is unknown to what extent briefly presented emotional words can be processed without awareness. By means of two independent functional magnetic resonance imaging studies, using either a block or an event-related design, we investigated brain activation to very briefly presented threat related and neutral words during two backward masking conditions (with and without gap between target and mask). In both experiments, emotional words were perceived during the supraliminal "with gap" condition, but they were not recognized during the subliminal "without gap" condition, as indicated by signal detection theory analysis. Imaging results of both experiments showed increased activation of the amygdala, the medial prefrontal cortex and language-processing cortical areas to negative versus neutral words during supraliminal but not subliminal conditions. These results suggest that even very briefly presented emotional words are capable of triggering increased cortical and subcortical processing; however, only when awareness of these stimuli is given.

Neural correlates of anticipation and processing of performance feedback in social anxiety.

Fear of negative evaluation, such as negative social performance feedback, is the core symptom of social anxiety. The present study investigated the neural correlates of anticipation and perception of social performance feedback in social anxiety. High (HSA) and low (LSA) socially anxious individuals were asked to give a speech on a personally relevant topic and received standardized but appropriate expert performance feedback in a succeeding experimental session in which neural activity was measured during anticipation and presentation of negative and positive performance feedback concerning the speech performance, or a neutral feedback-unrelated control condition. HSA compared to LSA subjects reported greater anxiety during anticipation of negative feedback. Functional magnetic resonance imaging results showed deactivation of medial prefrontal brain areas during anticipation of negative feedback relative to the control and the positive condition, and medial prefrontal and insular hyperactivation during presentation of negative as well as positive feedback in HSA compared to LSA subjects. The results indicate distinct processes underlying feedback processing during anticipation and presentation of feedback in HSA as compared to LSA individuals. In line with the role of the medial prefrontal cortex in self-referential information processing and the insula in interoception, social anxiety seems to be associated with lower self-monitoring during feedback anticipation, and an increased self-focus and interoception during feedback presentation, regardless of feedback valence.

Effects of social context on feedback-related activity in the human ventral striatum.

It is now well established that activation of the ventral striatum (VS) encodes feedback related information, in particular, aspects of feedback validity, reward magnitude, and reward probability. More recent findings also point toward a role of VS in encoding social context of feedback processing. Here, we investigated the effect of social observation on neural correlates of feedback processing. To this end, subjects performed a time estimation task and received positive, negative, or uninformative feedback. In one half of the experiment subjects thought that an experimenter closely monitored their face via a camera. We successfully replicated an elevated VS response to positive relative to negative feedback. Further, our data demonstrate that this reward-related activation of the VS is increased during observation by others. Using uninformative feedback as reference condition, we show that specifically VS activation during positive feedback was modulated by observation manipulation. Our findings support accounts which posit a role of VS in integrating social context into the processing of feedback and, in doing so, signaling its social relevance.

Effects of gaze direction, head orientation and valence of facial expression on amygdala activity.

There is increasing evidence for a role of the amygdala in processing gaze direction and emotional relevance of faces. In this event-related functional magnetic resonance study we investigated amygdala responses while we orthogonally manipulated head direction, gaze direction and facial expression (angry, happy and neutral). This allowed us to investigate effects of stimulus ambiguity, low-level factors and non-emotional factors on amygdala activation. Averted vs direct gaze induced increased activation in the right dorsal amygdala regardless of facial expression and head orientation. Furthermore, valence effects were found in the ventral amygdala and strongly dependent on head orientation. We observed enhanced activation to angry and neutral vs happy faces for observer-directed faces in the left ventral amygdala while the averted head condition reversed this pattern resulting in increased activation to happy as compared to angry and neutral faces. These results suggest that gaze direction drives specifically dorsal amygdala activation regardless of facial expression, low-level perceptual factors or stimulus ambiguity. The role of the amygdala is thus not restricted to the detection of potential threat, but has a more general role in attention processes. Furthermore, valence effects are associated with activation of the ventral amygdala and strongly influenced by non-emotional factors.

Automatic neural processing of disorder-related stimuli in social anxiety disorder: faces and more.

It has been proposed that social anxiety disorder (SAD) is associated with automatic information processing biases resulting in hypersensitivity to signals of social threat such as negative facial expressions. However, the nature and extent of automatic processes in SAD on the behavioral and neural level is not entirely clear yet. The present review summarizes neuroscientific findings on automatic processing of facial threat but also other disorder-related stimuli such as emotional prosody or negative words in SAD. We review initial evidence for automatic activation of the amygdala, insula, and sensory cortices as well as for automatic early electrophysiological components. However, findings vary depending on tasks, stimuli, and neuroscientific methods. Only few studies set out to examine automatic neural processes directly and systematic attempts are as yet lacking. We suggest that future studies should: (1) use different stimulus modalities, (2) examine different emotional expressions, (3) compare findings in SAD with other anxiety disorders, (4) use more sophisticated experimental designs to investigate features of automaticity systematically, and (5) combine different neuroscientific methods (such as functional neuroimaging and electrophysiology). Finally, the understanding of neural automatic processes could also provide hints for therapeutic approaches.

Amygdala activation to fearful faces under attentional load.

While some functional imaging studies suggested an automatic activation of the amygdala to fearful vs. neutral faces, recent studies showed the absence of amygdala activation to fearful faces under high attentional load induced by distracting tasks. The present fMRI study investigated whether this outcome can be modulated by changing the saliency of the eyes of fearful faces. Subjects had to solve a high perceptual load task while they were presented either with normal faces (Exp. 1) or with normal faces intermixed with faces, in which pupil and iris of eyes were erased to increase the saliency of the normal eyes (Exp. 2). There was no differential amygdala activation to fearful versus neutral faces under standard conditions without any manipulation of the faces (Exp. 1). In contrast to this outcome, Experiment 2 led to differential amygdala activation to the normal but not to the manipulated fearful vs. neutral faces. These findings propose a concept of relative automaticity of the activation of the amygdala. The activation depends on available cognitive resources and on the saliency of specific parts of fearful faces.

Processing of angry voices is modulated by visual load.

Visual perceptual load has been shown to modulate brain activation to emotional facial expressions. However, it is unknown whether cross-modal effects of visual perceptual load on brain activation to threat-related auditory stimuli also exist. The current fMRI study investigated brain responses to angry and neutral voices while subjects had to solve an easy or a demanding visual task. Although the easy visual condition was associated with increased activation in the right superior temporal region to angry vs. neutral prosody, this effect was absent during the demanding task. Thus, our results show that cross-modal perceptual load modulates the activation to emotional voices in the auditory cortex and that high visual load prevents the increased processing of emotional prosody.

Awareness modulates responses of the amygdala and the visual cortex to highly arousing visual threat.

It is still a matter of debate under which conditions the neural processing of emotional stimuli can occur without conscious awareness. Using functional magnetic resonance imaging, we investigated brain responses to highly arousing threat-related versus neutral pictures which were presented very briefly during two backward-masking conditions resulting in either subliminal or supraliminal stimulus processing. Signal detection analysis confirmed the successful experimental manipulation of awareness that effectively prevented stimulus recognition during the subliminal condition. Participants showed stronger responses of the amygdala and extrastriate visual cortex during the supraliminal, but not during the subliminal condition. These results suggest that the processing of highly arousing visual threat requires conscious awareness during backward masking. This contradicts the assumption of pervasive neural responses to emotional stimuli.

Neural mechanisms of the automatic processing of emotional information from faces and voices.

Theoretical accounts suggest an increased and automatic neural processing of emotional, especially threat-related, facial expressions and emotional prosody. In line with this assumption, several functional imaging studies showed activation to threat-related faces and voices in subcortical and cortical brain areas during attentional distraction or unconscious stimulus processing. Furthermore, electrophysiological studies provided evidence for automatic early brain responses to emotional facial expressions and emotional prosody. However, there is increasing evidence that available cognitive resources modulate brain responses to emotional signals from faces and voices, even though conflicting findings may occur depending on contextual factors, specific emotions, sensory modality, and neuroscientific methods used. The current review summarizes these findings and suggests that further studies should combine information from different sensory modalities and neuroscientific methods such as functional neuroimaging and electrophysiology. Furthermore, it is concluded that the variable saliency and relevance of emotional social signals on the one hand and available cognitive resources on the other hand interact in a dynamic manner, making absolute boundaries of the automatic processing of emotional information from faces and voices unlikely.

Visual attention modulates brain activation to angry voices.

In accordance with influential models proposing prioritized processing of threat, previous studies have shown automatic brain responses to angry prosody in the amygdala and the auditory cortex under auditory distraction conditions. However, it is unknown whether the automatic processing of angry prosody is also observed during cross-modal distraction. The current fMRI study investigated brain responses to angry versus neutral prosodic stimuli during visual distraction. During scanning, participants were exposed to angry or neutral prosodic stimuli while visual symbols were displayed simultaneously. By means of task requirements, participants either attended to the voices or to the visual stimuli. While the auditory task revealed pronounced activation in the auditory cortex and amygdala to angry versus neutral prosody, this effect was absent during the visual task. Thus, our results show a limitation of the automaticity of the activation of the amygdala and auditory cortex to angry prosody. The activation of these areas to threat-related voices depends on modality-specific attention.

Amygdala activation to threat under attentional load in individuals with anxiety disorder.

BACKGROUND: Previous studies in healthy subjects have shown that strong attentional distraction prevents the amygdala from responding to threat stimuli. Here, we investigated the effects of attentional load on amygdala activation to threat-related stimuli in individuals suffering from an anxiety disorder. METHODS: During functional magnetic resonance imaging, spider-phobicand healthy control subjects were presented with phobia-related and neutral stimuli while performing a distraction task with varying perceptual load (high vs low). RESULTS: Our data revealed a pattern of simultaneously increased amygdala and visual cortical activation to threat vs neutral pictures in phobic individuals, compared with controls, occurring regardless of attentional load. CONCLUSIONS: These results suggest that, in contrast to studies in healthy subjects, amygdala activation to clinically relevant threat stimuli is more resistant to attentional load.

The volatility of the amygdala response to masked fearful eyes.

Recently, it has been suggested that backwardly masked, and thus subliminally presented, fearful eyes are processed by the amygdala. Here, we investigated in four functional magnetic resonance imaging experiments whether the amygdala responds to subliminally presented fearful eyes per se or whether an interaction of masked eyes with the masks or with parts of the masks used for backward masking might be responsible for the amygdala activation. In these experiments, we varied the mask as well as the position of the target eyes. The results show that the amygdala does not respond to masked fearful eyes per se but to an interaction between masked fearful eyes and the eyes of neutral faces used for masking. This finding questions the hypothesis that the amygdala processes context-free parts of the human face without awareness.