The interaction between gaze and facial expression in the amygdala and extended amygdala is modulated by anxiety

Behavioral evidence indicates that angry faces are seen as more threatening, and elicit greater anxiety, when directed at the observer, whereas the influence of gaze on the processing of fearful faces is less consistent. Recent research has also found inconsistent effects of expression and gaze direction on the amygdala response to facial signals of threat. However, such studies have failed to consider the important influence of anxiety on the response to signals of threat; an influence that is well established in behavioral research and recent neuroimaging studies. Here, we investigated the way in which individual differences in anxiety would influence the interactive effect of gaze and expression on the response to angry and fearful faces in the human extended amygdala. Participants viewed images of fearful, angry and neutral faces, either displaying an averted or direct gaze. We found that state anxiety predicted an increased response in the dorsal amygdala/substantia innominata (SI) to angry faces when gazing at, relative to away from the observer. By contrast, high state anxious individuals showed an increased amygdala response to fearful faces that was less dependent on gaze. In addition, the relationship between state anxiety and gaze on emotional intensity ratings mirrored the relationship between anxiety and the amygdala/SI response. These results have implications for understanding the functional role of the amygdala and extended amygdala in processing signals of threat, and are consistent with the proposed role of this region in coding the relevance or significance of a stimulus to the observer

Personality influences the neural responses to viewing facial expressions of emotion

Cognitive research has long been aware of the relationship between individual differences in personality and performance on behavioural tasks. However, within the field of cognitive neuroscience, the way in which such differences manifest at a neural level has received relatively little attention. We review recent research addressing the relationship between personality traits and the neural response to viewing facial signals of emotion. In one section, we discuss work demonstrating the relationship between anxiety and the amygdala response to facial signals of threat. A second section considers research showing that individual differences in reward drive (behavioural activation system), a trait linked to aggression, influence the neural responsivity and connectivity between brain regions implicated in aggression when viewing facial signals of anger. Finally, we address recent criticisms of the correlational approach to fMRI analyses and conclude that when used appropriately, analyses examining the relationship between personality and brain activity provide a useful tool for understanding the neural basis of facial expression processing and emotion processing in general

Trait anxiety modulates anterior cingulate activation to threat interference

Background: Individuals vary in the degree to which salient threatening stimuli disrupt or distract from goal-directed cognitive processes. Excessive attention to threat or difficulty resolving the interference created by threat cues could contribute to anxious psychopathology; disruptions in frontal brain regions implicated in attentional control or resolution of emotional interference (e.g. anterior cingulate cortex, “ACC”) might play a role. In this study, we explored the hypothesis that trait anxiety would be associated with ACC activity in an attentional control task with varying levels of threat interference. Methods: During functional magnetic resonance imaging, 20 healthy individuals who varied in trait anxiety levels viewed angry, fearful, and neutral faces superimposed on an indoor or outdoor scene. In a high-threat interference condition, subjects identified the gender of the face (Attend Face). In a low-threat interference condition, they identified the scene type (Attend Scene). Whole-brain analysis was used to compare Attend Face with Attend Scene for angry and fearful (versus neutral) faces. Contrasts were correlated with trait anxiety level. Results: Behavioral data confirmed that Attend Face produced greater threat interference than Attend Scene. Brain imaging results showed that trait anxiety was inversely associated with bilateral rostral ACC activity for Attend Face relative to Attend Scene for angry faces. A similar relationship was not seen for fearful faces. Conclusions: The rostral ACC is implicated in assessing the salience of emotional information and controlling attention to resolve emotional interference. The link between higher trait anxiety and decreased ACC activation for angry faces suggests reduced attentional control for signals of interpersonal threat in healthy anxiety-prone individuals. Depression and Anxiety 28:194–201, 2011. © 2011 Wiley-Liss, Inc.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/83482/1/20802_ftp.pd

An investigation into the emotion-cognition interaction and sub-clinical anxiety

This thesis combines behavioural and electrophysiological approaches in the study of the emotion-cognition interaction and sub-clinical anxiety. The research questions addressed in this thesis concern, specifically: the impact of emotion on attention; the interplay between attention and emotion in anxiety;and the cognitive construct of affect. Chapter 1 provides an introduction to emotion research, cognitive models of anxiety and motivates the thesis. Chapter 2 investigates whether affective processing is automatic. More specifically, to elucidate whether facilitated processing of threat in anxiety, evidenced by emotion-related ERP modulations, requires attentional resources. It was previously reported that emotional expression effects on ERP waveforms were completely eliminated when attention was directed away from emotional faces to other task-relevant locations (Eimer et al., 2003). However, Bishop et al. (2004) reported that threat-related stimuli can evoke amygdala activity without attentional engagement or conscious awareness in high-anxious but not low-anxious participants. Spatial attention was manipulated using a similar paradigm as Vuilleumier et al. (2001) and Holmes et al. (2003), to investigate the mechanism underlying the threat-related processing bias in anxiety by examining the influence of spatial attention and trait anxiety levels on established ERP modulations by emotional stimuli. Participants were instructed to match two peripheral faces or two peripheral Landolt squares. The Landolt squares task was selected since this is an attentionally demanding task and would likely consume most, if not all, attention resources. The ERP data did not offer support to the claim that affective stimuli are processed during unattended conditions in high-anxious but not low-anxious participants. Rather, it questions whether a preattentive processing bias for emotional faces is specific to heightened anxiety. This is based on the finding of an enhanced LPP response for threat/happy versus neutral faces and an enhanced slow wave for threat versus neutral faces, neither modulated by the focus of attention for both high and low anxiety groups. Chapter 3 investigated the delayed disengagement hypothesis proposed by Fox and colleagues (2001) as the mechanism underlying the threat-related attentional bias in anxiety. This was done by measuring N2pc and LRP latencies while participants performed an adapted version of the spatial cueing task.Stimuli consisted of a central affective image (either a face or IAPS picture, depending on condition) flanked to the left and right by a letter/number pair. Participants had to direct their attention to the left or right of a central affective image to make an orientation judgement of the letter stimulus. It was hypothesised that if threat-related stimuli are able to prolong attentional processing, N2pc onset should be delayed relative to the neutral condition. However, N2pc latency was not modulated by emotional valence of the central image, for either high or low anxiety groups. Thus, this finding does not provide support for the locus of the threat-related bias to the disengage component of attention. Chapter 4 further investigated the pattern of attentional deployment in the threat-related bias in anxiety. This was done by measuring task-switching ability between neutral and emotional tasks using an adapted version of Johnson’s (in press) attentional control capacity for emotional representations (ACCE) task. Participants performed either an emotional judgement or a neutral judgement task on a compound stimulus that consisted of an affective image (either happy versus fearful faces in the faces condition, or positive versus negative IAPS pictures in the IAPS condition) with a word located centrally across the image (real word versus pseudo-word). Participants scoring higher in trait anxiety were faster to switch from a neutral to a threatening mental set. This improved ability to switch attention to the emotional judgement task when threatening faces are presented is in accordance with a hypervigilance theory of anxiety. However, this processing bias for threat in anxiety was only apparent for emotional faces and not affective scenes, despite the fact that pictures depicting aversive threat scenes were used (e.g., violence, mutilation). This is discussed in more detail with respect to the social significance of salient stimuli. Chapter 5 in a pair of experiments sought to investigate how affect is mentally represented and specifically questions whether affect is represented on the basis of a conceptual metaphor linking direction and affect. The data suggest that the vertical position metaphor underlies our understanding of the relatively abstract concept of affect and is implicitly active, where positive equates with ‘upwards’ and negative with ‘downwards’. Metaphor-compatible directional movements were demonstrated to facilitate response latencies, such that participants were relatively faster to make upward responses to positively-evaluated words and downward responses to negatively-evaluated words than to metaphorincompatible stimulus-response mappings. The finding suggests that popular use of linguistic metaphors depicting spatial representation of affect may reflect our underlying cognitive construct of the abstract concept of valence. Chapter 6 summarises the research in the thesis and implications of the present results are discussed, in particular in relation to cognitive models of anxiety. Areas of possible future research are provided

Association between Ability Emotional Intelligence and Left Insula during Social Judgment of Facial Emotions

The human ability of identifying, processing and regulating emotions from social stimuli is generally referred as Emotional Intelligence (EI). Within EI, Ability EI identifies a performance measure assessing individual skills at perceiving, using, understanding and managing emotions. Previous models suggest that a brain "somatic marker circuitry" (SMC) sustains emotional sub-processes included in EI. Three primary brain regions are included: the amygdala, the insula and the ventromedial prefrontal cortex (vmPFC). Here, our aim was to investigate the relationship between Ability EI scores and SMC activity during social judgment of emotional faces. Sixty-three healthy subjects completed a test measuring Ability EI and underwent fMRI during a social decision task (i.e. approach or avoid) about emotional faces with different facial expressions. Imaging data revealed that EI scores are associated with left insula activity during social judgment of emotional faces as a function of facial expression. Specifically, higher EI scores are associated with greater left insula activity during social judgment of fearful faces but also with lower activity of this region during social judgment of angry faces. These findings indicate that the association between Ability EI and the SMC activity during social behavior is region- and emotionspecific.Peer reviewe

Decoding Unattended Fearful Faces with Whole-Brain Correlations: An Approach to Identify Condition-Dependent Large-Scale Functional Connectivity

Processing of unattended threat-related stimuli, such as fearful faces, has been previously examined using group functional magnetic resonance (fMRI) approaches. However, the identification of features of brain activity containing sufficient information to decode, or “brain-read”, unattended (implicit) fear perception remains an active research goal. Here we test the hypothesis that patterns of large-scale functional connectivity (FC) decode the emotional expression of implicitly perceived faces within single individuals using training data from separate subjects. fMRI and a blocked design were used to acquire BOLD signals during implicit (task-unrelated) presentation of fearful and neutral faces. A pattern classifier (linear kernel Support Vector Machine, or SVM) with linear filter feature selection used pair-wise FC as features to predict the emotional expression of implicitly presented faces. We plotted classification accuracy vs. number of top N selected features and observed that significantly higher than chance accuracies (between 90–100%) were achieved with 15–40 features. During fearful face presentation, the most informative and positively modulated FC was between angular gyrus and hippocampus, while the greatest overall contributing region was the thalamus, with positively modulated connections to bilateral middle temporal gyrus and insula. Other FCs that predicted fear included superior-occipital and parietal regions, cerebellum and prefrontal cortex. By comparison, patterns of spatial activity (as opposed to interactivity) were relatively uninformative in decoding implicit fear. These findings indicate that whole-brain patterns of interactivity are a sensitive and informative signature of unattended fearful emotion processing. At the same time, we demonstrate and propose a sensitive and exploratory approach for the identification of large-scale, condition-dependent FC. In contrast to model-based, group approaches, the current approach does not discount the multivariate, joint responses of multiple functional connections and is not hampered by signal loss and the need for multiple comparisons correction

Effect of trait anxiety on prefrontal control mechanisms during emotional conflict

International audienceConverging evidence points to a link between anxiety proneness and altered emotional functioning, including threat-related biases in selective attention and higher susceptibility to emotionally ambiguous stimuli. However, during these complex emotional situations, it remains unclear how trait anxiety affects the engagement of the prefrontal emotional control system and particularly the anterior cingulate cortex (ACC), a core region at the intersection of the limbic and prefrontal systems. Using an emotional conflict task and functional magnetic resonance imaging (fMRI), we investigated in healthy subjects the relations between trait anxiety and both regional activity and functional connectivity (psychophysiological interaction) of the ACC. Higher levels of anxiety were associated with stronger task-related activation in ACC but with reduced functional connectivity between ACC and lateral prefrontal cortex (LPFC). These results support the hypothesis that when one is faced with emotionally incompatible information, anxiety leads to inefficient high-order control, characterized by insufficient ACC-LPFC functional coupling and increases, possibly compensatory, in activation of ACC. Our findings provide a deeper understanding of the pathophysiology of the neural circuitry underlying anxiety and may offer potential treatment markers for anxiety disorders

Amygdala response to emotional stimuli without awareness: Facts and interpretations

Over the past two decades, evidence has accumulated that the human amygdala exerts some of its functions also when the observer is not aware of the content, or even presence, of the triggering emotional stimulus. Nevertheless, there is as of yet no consensus on the limits and conditions that affect the extent of amygdala\u2019s response without focused attention or awareness. Here we review past and recent studies on this subject, examining neuroimaging literature on healthy participants as well as brain damaged patients, and we comment on their strengths and limits. We propose a theoretical distinction between processes involved in attentional unawareness, wherein the stimulus is potentially accessible to enter visual awareness but fails to do so because attention is diverted, and in sensory unawareness, wherein the stimulus fails to enter awareness because its normal processing in the visual cortex is suppressed. We argue this distinction, along with data sampling amygdala responses with high temporal resolution, helps to appreciate the multiplicity of functional and anatomical mechanisms centered on the amygdala and supporting its role in non-conscious emotion processing. Separate, but interacting, networks relay visual information to the amygdala exploiting different computational properties of subcortical and cortical routes, thereby supporting amygdala functions at different stages of emotion processing. This view reconciles some apparent contradictions in the literature, as well as seemingly contrasting proposals, such as the dual stage and the dual route model. We conclude that evidence in favor of the amygdala response without awareness is solid, albeit this response originates from different functional mechanisms and is driven by more complex neural networks than commonly assumed. Acknowledging the complexity of such mechanisms can foster new insights on the varieties of amygdala functions without awareness and their impact on human behavior

Individual differences in anxiety and automatic amygdala response to fearful faces: A replication and extension of Etkin et al. (2004)

Trait anxiety refers to the stable tendency to attend to threats and experience fears and worries across many situations. According to the widely noticed, pioneering investigation by Etkin et al. (2004) trait anxiety is strongly associated with reactivity in the right basolateral amygdala to non-conscious threat. Although this observation was based on a sample of only 17 individuals, no replication effort has been reported yet. We reexamined automatic amygdala responsiveness as a function of anxiety in a large sample of 107 participants. Besides self-report instruments, we administered an indirect test to assess implicit anxiety. To assess early, automatic stages of emotion processing, we used a color-decision paradigm presenting brief (33 ms) and backward-masked fearful facial expressions. N = 56 participants were unaware of the presence of masked faces. In this subset of unaware participants, the relationship between trait anxiety and basolateral amygdala activation by fearful faces was successfully replicated in region of interest analyses. Additionally, a relation of implicit anxiety with masked fear processing in the amygdala and temporal gyrus was observed. We provide evidence that implicit measures of affect can be valuable predictors of automatic brain responsiveness and may represent useful additions to explicit measures. Our findings support a central role of amygdala reactivity to non-consciously perceived threat in understanding and predicting dispositional anxiety, i.e. the frequency of spontaneously occurring anxiety in everyday life