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Individual differences in emotion processing
Recent research in the Social and Affective Neuroscience group has been concerned with exploring individual differences in the way we process emotions. Several examples of our ongoing research in this area are listed below.
Aggression
Anxiety/Fear
Response to Food/Reward
Aggression
Neural response to angry faces is modulated by trait reward drive
Beaver, J. D., Lawrence, A. W., Passamonti, L., & Calder, A. J. (2008). Appetitive motivation predicts the neural response to facial signals of aggression. The Journal of Neuroscience, 12, 2719 –2725.
The 'Behavioural Approach System' (BAS) (Gray, 1990) has been primarily associated with reward processing and positive affect. However, additional research has demonstrated that the BAS plays a role in aggressive behaviour, heightened experience of anger, and increased attention to facial signals of aggression. Using fMRI, we showed that variation in the BAS trait in healthy participants predicts activation in neural regions implicated in aggression when participants view facial signals of aggression in others. Increased BAS-drive (appetitive motivation) was associated with increased amygdala activation and decreased ventral anterior cingulate and ventral striatal activation to facial signals of aggression, relative to sad and neutral expressions. In contrast, increased Behavioural Inhibition (BIS) was associated with increased activation in the dorsal anterior cingulate, a region involved in the perception of fear and threat. Our results provide the first demonstration that appetitive motivation constitutes a significant factor governing the function of neural regions implicated in aggression, and have implications for understanding clinical disorders of aggression.
Figure 1. Neural response to angry faces is positively correlated with individual differences in reward drive in the amygdala (left) and negatively correlated with this dimension in the ventral anterior cingulate (right).
Reward drive modulates prefrontal cortex-amygdala connectivity during processing of angry faces
Passamonti, L., Rowe, J. B., Ewbank, M.P., Hampshire, A., Keane, J. & Calder, A., J. (2008). Connectivity from the ventral anterior cingulate to the amygdala is modulated by appetitive motivation in response to facial signals of aggression. Neuroimage, 15, 562-70.
Our previous experiment showed that reward drive modulates the isolated response in the amygdala and the ventral anterior cingulate (vACC) when viewing angry faces; however, this study did not explore important interactions that could occur between these regions. In a new experiment, we therefore investigated whether viewing angry vs. neutral faces was associated with changes in connectivity between the amygdala and the vACC, using a method called PsychoPhysiological Interactions (PPI). We also investigated the directionality of any connectivity effect (i.e. from the vACC to the amygdala, rather than vice versa or a bidirectional effect) with a different, but complementary, approach known as Dynamic Causal Modelling (DCM). Both PPI and DCM demonstrated that the connectivity between the vACC and the amygdala was strongly correlated with personality, with high-reward drive individuals displaying reduced negative connectivity. Furthermore, the direction of this effect was restricted from the vACC to the amygdala but not vice versa. The variation in the connectivity pattern from the vACC to the amygdala can represent a brain marker of altered emotional regulation in subjects with enhanced tendency to display aggressive behaviour. In future, specific neurobiological markers could be used to detect individuals at increased risk for psychiatric disorders.
PsychoPhysiological Interactions (PPI). (A) Either an angry or neutral face was presented on each trial. (B) The amygdala ('source') was defined as a 10 mm sphere. (C) The vACC changes its connectivity pattern (i.e. correlation) with the amygdala as a function of both viewing angry vs. neutral faces and of the reward drive personality. (D) Data plot from C. High-reward drive showed reduced negative change in connectivity compared with low-reward drive individuals.
Dynamic Causal Modelling (DCM). Reward drive is significantly correlated with the effect of emotion (B value— angry vs. neutral) on the connectivity from the vACC to the amygdala (B2,1) but not vice versa (B1,2). In contrast, there is no relationship between reward drive and the effect of faces per se on both amygdala and vACC (C values— regardless of the emotions).
Anxiety/Fear
Collaborative research between members of the Emotion and Attention groups has focused upon the neural substrate of selective attention to threat and its modulation by attention. Initial investigation of the influence of anxiety upon the neural response to fearful versus neutral face distractors was conducted by Sonia Bishop (now at UC Berkeley), Andrew Lawrence (now at University of Cardiff) and John Duncan.
Anxiety predicts the amygdala response to unattended fearful faces
Bishop, S.J., Duncan, J., Lawrence, A.D. (2004) State Anxiety modulation of the amygdala response to unattended threat-related stimuli. Journal of Neuroscience, 24, 10364-8 .pdf
A number of studies have examined whether the amygdala response to threat is modulated by attention, but with mixed results. Cognitive studies of anxiety have shown that attentional biases towards threat-related stimuli vary dramatically between high anxious and low anxious individuals, yet this is often overlooked in neuroimaging studies. We attempted to investigate the influence of anxiety on the neural response to threat across a series of studies. The first of these examined whether anxiety influences attentional modulation of the amygdala response to fearful faces. In an event-related fMRI paradigm, participants performed a matching task on pairs of houses and faces appearing in attended or unattended locations. Faces could either show a fearful or neutral expression. We found that only high anxious, and not low anxious, individuals showed an amygdala response to unattended fearful faces while both high and low anxious individuals showed an amygdala response to attended threat stimuli.
Figure 2. Example stimuli. On each trial, two faces and two houses were presented in vertical and horizontal pairs around a central fixation cross. Participants matched either faces or houses, as cued by spatial location. Faces could differ in identity, but both were always either neutral or fearful in expression.
Figure 3. Anxiety influences attentional modulation of amygdala activity to fearful versus neutral faces. (a) Amygdala activity to attended fearful faces (AF) vs attended neutral faces (AN) relative to unattended fearful faces (UF) vs unattended neutral faces (UN) against state anxiety (STAI). Activation plotted is mean signal change associated with this contrast for the peak voxel from the left amygdala ROI, x, y, z = -18 -10 20, Z = 2.80, P-corrected < 0.02. (b) Amygdala activity to fearful versus neutral faces by attentional condition and anxiety level. Participants were divided into 'low' and 'high' anxious groups using a median split on STAI scores. Amygdala activity is mean signal change for the peak voxel from (a). (Taken from Bishop et al. 2004. J Neurosci.),
In more recent work, we have expanded upon these findings by focusing on the way in which the attentional focus of the observer, and the expresser, can influence the neural response to facial signals of different negative emotional expressions – including anger as well as fear.
Differential effects of anxiety and attention on the amygdala response to anger and fear
Ewbank M.P., Lawrence, A.D. Passamonti, L. Keane, J. Peers, P.V. & Calder, A.J. (In Press) Differential effects of anxiety and attention on the amygdala response to facial signals of anger and fear. NeuroImage.
Angry facial expressions also represent a potent, yet qualitatively different form of threat to that signalled by fearful faces. While fearful faces are thought to signal the presence of a significant, yet undetermined source of danger within the environment, referred to as 'ambiguous threat', angry faces represent a more direct form of threat, often used in face-to-face encounters to exert dominance. In order to investigate the influence of anxiety and attention on the neural response to different forms of threat we used an identical paradigm to that used in the previous study, with the additional inclusion of angry as well as fearful and neutral faces. In line with the inherent differences between anger and fear, we precited that anxiety would modulate the amygdala response to angry faces to a greater extent when attended. Higher anxiety levels produced an increased amygdala response to angry faces (relative to neutral or fearful faces) when attended, but not unattended. By contrast, increased anxiety was associated with a greater amygdala response to fearful faces (relative to neutral or angry faces) in the unattended condition, with only borderline evidence for attended fear (relative to neutral). These findings demonstrate different effects of attention and anxiety on the amygdala responses to facial signals of fear and aggression, consistent with the different nature of threat signalled by these expressions.
Figure 4. (A) Correlation between amygdala activation and anxiety for attended angry faces compared to attended neutral faces (B) attended angry faces compared to attended fearful faces (C) unattended fearful faces compared to unattended neutral faces, and (D) unattended fearful faces compared to unattended angry faces. All are thresholded at P<0.002 uncorrected (10 contiguous voxels).
Influence of eye gaze direction and anxiety on the amygdala response to anger and fear
Ewbank, M.P., Nummenmaa, L., Calder, A.J. (2008) The role of eye gaze and anxiety on the amygdala response to angry and fearful faces, 10th International Conference in Cognitive Neuroscience, Bodrum, Turkey.
Having explored the influence of the observer's attention on the response to facial signals of anger and fear, we were specifically interested in addressing how anxiety influences the contrasting relationship; namely that between the facial expression and direction of attention of the expresser. The particularly interpersonal nature of facial signals of anger suggests the relevance of threat signalled by this expression may differ depending upon the where the expresser is looking. Indeed, numerous studies suggest that the perception of an angry face is enhanced when the face presents a direct (or mutual) gaze. Evidence is inconclusive however, as to the role of gaze in the perception of fearful faces. Participants viewed images of fearful, angry and neutral faces, either displaying an averted or mutual gaze. Anxiety and gaze produced differential effects on the amygdala response to angry and fearful faces. Anxiety predicted an increased response to fearful faces when directed towards or away from the observer. By contrast, high anxious individuals showed an increased amygdala response to angry faces only when gaze was directed towards them. Thus, in contrast to fear, the amygdala response to anger was dependent upon gaze direction. These results accord with the proposed role of the amygdala as coding biologically relevant stimuli.
Response to Food/Reward
Individual differences in reward drive predict neural response to images of food
Beaver, J. D., Lawrence, A. D., van Ditzhuijzen, J., Davis, M. H., Woods, A., & Calder, A. J. (2006). Individual differences in reward drive predict neural responses to images of food. Journal of Neuroscience, 26(19), 5160–5166.
Comparative research has demonstrated the involvement of a network of brain regions—orbitofrontal cortex, ventral striatum, amygdala, hypothalamus and midbrain areas—in food reward. Functional MRI revealed that areas of this network—including the ventral striatum, orbitofrontal cortex, and amygdala—were activated when individuals viewed pictures of high-calorie appetising foods (e.g., chocolate cake, pizza) relative to bland foods (e.g., potatoes, plain rice). Behavioural research has shown that individuals with high trait sensitivity to reward experience more frequent and intense food cravings and are more likely to be overweight or develop eating disorders associated with excessive food intake (Davis, Strachan, & Berkson, 2004; Davis & Woodside, 2002). Hence, it is particularly interesting that individual variation in the neural response to food images was significantly correlated with individual differences in trait reward drive. Individuals with higher reward drive (i.e. a greater tendency to pursue reward) displayed greater responses to images of appetising foods in a fronto-amygdala-ventral striatal-midbrain network. These results demonstrate that the neural response to food cues is influenced by individual differences in reward drive and may provide insight into individual vulnerability to certain eating problems (e.g. overeating).
Figure 5. Ventral striatum response to viewing of appetising food images relative to bland food images.
Figure 6. BOLD signal change in peak activated voxels in the reward network for appetising relative to bland foods plotted as a function of individual trait reward drive.
Brain markers of a risk factor for obesity: External Food Sensitivity
Passamonti, L., Rowe, J.B., Schwarzbauer, C., Ewbank, M.P., von dem Hagen, E., & Calder, A.J. (2009). Personality predicts the brain's response to viewing appetizing foods: the neural basis of a risk factor for overeating. Journal of Neuroscience, 7, 43-51.
In addition to reward-drive, we also identified how another risk factor for overeating, the "External Food Sensitivity" (EFS), predicts brain responses when viewing pictures of foods. EFS personality trait reflects how much the feeding behaviour is driven by external cues (i.e. how appetizing the food appears). Eating is indeed not only triggered by hunger but also by the sight of foods, and viewing appetizing foods alone can induce food craving and overeating. Previous comparative research indicated that the connectivity or 'communication' between the amygdala, ventral striatum (nucleus accumbens) and the prefrontal cortex is modulated when animals are exposed to contextual cues associated with food. Using fMRI, we showed that viewing appetizing food produced changes in the connectivity between analogous brain regions in humans that were strongly correlated with individual differences in EFS. Variations in dynamic interactions within the human feeding network might determine the individual's risk for overeating. Given recent concerns that advertisements and packaging can initiate and maintain increased food intake, identifying the neurobiological basis of EFS is crucial for understanding obesity.
This research has also been covered on the media at www.msnbc.msn.com/id/28794584/ and www.wellcome.ac.uk/News/2009/News/WTX053024.htm
Figure 7. The connectivity between the amygdala and ventral striatum (thought to reflect emotional states evoked by the sight of appetizing foods) and the connectivity between the ventral striatum and the orofacial region of the premotor cortex (representing the preparation of motor acts necessary for eating) are both positively correlated with EFS (red solid lines). In contrast, EFS is negatively associated with the connectivity between the dorsal/ventral ACC and amygdala and between the dorsalACC and the ventral striatum (red dotted lines) which are interpreted as abnormal prefrontal–limbic interactions.