You are in: Home » Research at the Unit » Emotion research
Neural substrates of basic emotions
Neuropsychology of emotion
In addition to the researchers mentioned in each section, a number of studies have also been conducted in collaboration with Andy Young (University of York), Dave Perrett (University of St Andrews), and Andrew Lawrence(Cardiff).
Research discussed below addressing the neural underpinnings of fear and disgust are summarised in a review article - 'The Neuropsychology of Fear and Loathing' (Calder, Lawrence, and Young, 2001b; Nature Reviews Neuroscience, 2(5), 352-363). Here we argue that brain mechanisms underlying these two emotions are coded by separate, but overlapping systems. A system for fear in which the amygdala appears to be critical, and another for disgust in which the important neural structures are the insula and parts of the basal ganglia (Figure 1).
Impaired recognition of fear and anger following bilateral amygdala damage
An investigation of two cases with bilateral amygdala damage, DR and SE revealed that both have problems in recognising facial expressions of fear, and to a lesser extent anger (Calder et al., 1996b). Additional collaborative projects with Ralph Adolphs (Caltech, USA) and Paul Broks (Plymouth), have confirmed the amygdala's role in processing facial expressions of emotion, and in particular fear (Adolphs et al., 1999; Broks et al., 1998).
A collaborative project with Sophie Scott (University College London), addressed the contribution of the amygdala to the recognition of emotion from vocal cues (Scott et al., 1997) in case DR. Results showed that DR demonstrates an identical pattern in the vocal domain (i.e., impaired recognition of vocal signals of fear and anger), supporting the view that the amygdala contributes to the recognition of these emotions across different sensory modalities (Calder et al., 2001b). This proposal is also supported by a collaborative functional imaging (fMRI) project with Mary Phillips (Institute of Psychiatry) (Phillips et al., 1998), which showed enhanced amygdala signals for facial and vocal signals of fear (see below).
A Neural Response in the Human Amygdala to Fearful Facial Expressions
Collaborative projects with Ray Dolan at the Wellcome Department of Cognitive Neurology, used Positron Emission Tomography (PET) to investigate participants' perception of different intensities of facial expressions of fear and happiness (see perception of facial expressions page) (Figure 2) (Morris et al, 1996; 1998). The results demonstrated that fear, but not happy facial expressions produced increased rCBF in the amygdala. Moreover, activation in the amygdala was positively correlated with increasing intensity of facial expressions of fear, and negatively correlated with increasing intensity of facial expressions of happiness (Figure 3).
Figure 2: The two image sequences show examples of the morphed continua used. The sequences ranged between neutral and afraid (top) and neutral and happy (bottom) expressions (100%), and then beyond to caricatured (125%) versions of each expression. Participants viewed examples of the images in a block design. Different levels of exaggeration of each emotion were presented in separate blocks (i.e., 25% fear images, 75% happy images were shown in separate blocks).
Figure 3: Activation in the amygdala showed a linear relationship with decreasing intensity of happiness and increasing intensity of fear (see Figure 2). A fear minus happy contrast also showed increased rCBF in the amygdala.
Impaired recognition of disgust
Collaborative work with Reiner Sprengelmeyer has demonstrated that Huntington's disease causes a disproportionate impairment in recognising facial expressions of disgust (Sprengelmeyer et al., 1996; Sprengerlmeyer et al., 1997). To investigate further the role of the basal ganglia in coding this emotion, an additional project examined two psychiatric disorders associated with abnormal metabolic activity in this brain region - obsessive compulsive disorder (OCD) and Gilles de la Tourette syndrome (Braun et al., 1995; Rapoport, 1989; Rapoport & Fiske, 1998). The results showed that the OCD group and sub-group of the Tourette's group with co-morbid OCD symptoms showed a selective impairment in recognising disgust facial expressions. These findings emphasise the role of the basal ganglia in recognising disgust. In addition, it was proposed that the presence of OCD symptoms in the patients' childhood years may have led to a weakened mapping between self-experienced emotion and the facial expressions of others.
Functional imaging studies of disgust
Huntington's disease, OCD and Tourette's syndrome are not characterised by focal neuropathology. Hence, although these patient-based studies point towards the probable involvement of the basal ganglia in disgust, the evidence is indirect. In this respect functional imaging research has been particularly informative. Collaborative work with Mary Phillips (IOP) (Phillips et al., 1998; Phillips et al., 1997) has identified two areas involved in processing facial expressions of disgust - the insula and the basal ganglia (Figures 4&5). Insula involvement is particularly interesting given its identified role in gustatory function (Augustine, 1996; Small et al., 1999). Of equal relevance is research showing that lesions to the insula or pallidum of rats interferes with conditioned taste aversion (Dunn & Everitt, 1988; Hernadi, Zaradi, Faludi, & Lenard, 1997). Together these findings concur with Rozin and colleagues' (Rozin & Fallon, 1987; Rozin, Lowery, & Ebert, 1994) proposal that disgust has developed from a more primitive system involved in distaste.
Figure 4: Examples of stimuli used by Phillips et al (1997). Two levels of disgust and fear expressions were used â€" morphed (blended) images containing 75% of the expression and 25% neutral, and 150% caricatures of the expressions (see perception of facial expressions page). The baseline condition contained morphs composed of 25% happiness and 75% neutral.
Figure 5: Left - the neural correlates of viewing disgust facial expressions (disgust minus baseline [25% happy condition]) for both 75% and 150% disgust images. Both show significant signals in the insula and basal ganglia. Right â€" anterior insula activation associated with the 150% disgust minus 75% disgust contrast. Contrasts involving the fear expressions replicated the involvement of the amygdala discussed above (Figure 3).
A cross-model system for recognising disgust
We have provided further evidence for the role of the insula/basal ganglia regions in processing disgust in the form of a case study of a man (NK) with a focal lesion affecting these areas (Calder, Keane, Manes, Antoun, & Young, 2000b). NK's damage is lateralised to the left and includes the insula, putamen, internal capsule, globus pallidus, and the head of the caudate (Figure 6). NK showed highly selective impairments in recognising disgust from facial and vocal cues; his self-reported experience of disgust was also significantly reduced. NK's results are consistent with damage to a system involved in both the recognition of disgust from different sensory modalities and the experience of this emotion.
Figure 6: Axial (left) and coronal (right) T1-weighted MR images showing a left hemisphere infarction involving the posterior part of the anterior insula, posterior insula, internal capsule, the putamen and the globus pallidus. Coronal (right) image also shows damage to the head of the caudate nucleus. To aid interpretation, the intact right putamen (P) and intact right globus pallidus (GP) (axial section (left)), and intact right head of caudate (CN) (coronal section (right)) have been traced. Insula lesion is identified by a white arrow (I).
Differential effects of ageing on the recognition of fear and disgust
In line with the proposal that separate neural systems underlie the recognition of fear and disgust, we have found differential effects of ageing on the recognition of these emotions (Calder et al., 2002). On two tests of facial expression recognition with five age groups ranging from 20-30 years to 60-70 years, increasing age produced a progressive reduction in the recognition of fear and, to a lesser extent, anger. In contrast, older participants showed absolutely no reduction in recognition of facial expressions of disgust, rather there was evidence of an improvement. Recognition of other facial expressions showed no significant evidence of deterioration (or enhancement) across age groups. These results are consistent with the differential effects of ageing on two brain regions underlying the recognition of fear and disgust. In relation to fear, research has shown that medial temporal pathology (including the amygdala) is a consequence of normal ageing (Anderton, 1997), while fMRI research has demonstrated reduced amygdala activation to negative facial expressions with increasing age (Iidaka et al., 2001). In contrast, the gross structure and neurochemistry of a region of the basal ganglia implicated in taste aversion (Hernadi et al., 1997), OCD, and fMRI studies of disgust (Calder et al., 2002), is largely spared by ageing (Raz, 2000).
The contribution of frontal systems to facial expression recognition
The work discussed above identifies separate neural mechanisms involved in processing fear (amygdala) and disgust (insula and basal ganglia). Other studies, however, have emphasised the important role of the frontal lobes in processing emotional cues in general, and some have suggested that the systems involved in coding individual emotions may feed into more general emotion systems in frontal cortex (Sprengelmeyer, Rausch, Eysel, & Przuntek, 1998). If this is correct, then we would expect to see general emotion recognition impairments following frontal cortex damage. We recently investigated this issue in a case series of patients with frontal variant frontotemporal dementia (fvFTD) (Keane, Calder, Hodges, & Young, 2002), a condition that largely affects the frontal regions of the brain but particularly the ventromedial frontal lobes. The results showed that fvFTD was associated with impaired recognition of a number of emotions from both facial and auditory cues. In contrast, there was no evidence of impaired recognition of identity from faces. These results emphasise a role for the frontal lobes in processing emotional cues from different sensory modalities. In addition, they suggest that previous reports of impaired facial expression recognition in the absence of impaired facial identity recognition, may have been incorrect to interpret this pattern as the antithesis of prosopagnosia (impaired facial identity recognition). Rather, as suggested by the results of the fvFTD study, this pattern may instead reflect impaired recognition of emotion.
Perceptual and motor codes involved in facial expression recognition
It is tempting to think of the perceptual mechanisms underlying facial expression recognition as analogous to those for facial identity. However, we should be cautious of adopting this view for a number of reasons. Foremost amongst these is that we not only recognise expressions in other people's faces, we generate them ourselves. Hence, in addition to a visual code, the mental representation of facial expressions has the added requirement of a motor-program code (to produce the expression). The extent to which these two codes interact is unclear. To investigate this issue, we studied a group of participants with a rare congenital disorder that causes facial diplegia (Möbius Syndrome) (Calder, Keane, Cole, Campbell, & Young, 2000a), meaning that they have never produced facial expressions. Anecdotal reports had suggested that this group are severely impaired at recognising facial expressions, but until now, there has been no systematic research. We found no evidence of marked deficits in facial expression recognition in the Möbius individuals. These findings demonstrate that there is minimal interaction between motor-code and visual representations for facial expression recognition.
Eye gaze processing
We have explored the role of eye gaze in social interaction using functional imaging (PET) (Calder et al., 2002). This initial study investigated Baron-Cohen's (1997) proposal that the interpretation of gaze plays an important role in a normal functioning theory of mind (ToM) system. Consistent with this proposal, previous functional imaging research has shown that both ToM and eye gaze tasks engage a similar region of posterior superior temporal sulcus (STS). However, a second, more prominent brain region associated with ToM, the medial prefrontal (MPF) cortex, had not been identified by the eye gaze research. Certain methodological issues that might account for the absence of MPF activation in these experiments were identified, and a PET study that controlled for these factors addressed the neural correlates of processing direct and averted gaze. The results showed that the MPF regions associated with ToM were indeed involved in processing gaze, but particularly averted gaze (Figure 7). Moreover, because participants were not explicitly asked to attend to the faces' gaze, the study demonstrates that simply viewing a face with averted gaze is sufficient to engage the mechanisms involved in ToM.
Figure 7: Medial frontal region (BA 8/9) involved in viewing faces with averted gaze.
Selective impairment in anger recognition
A collaborative project with Andrew Lawrence (CBU) investigated the neurochemical basis of emotion perception. Offensive aggression occurs in the context of resource/dominance disputes in a wide variety of species. Hence, the possibility arises that a specific neural system may have evolved to detect and coordinate responses to this specific form of threat. The dopamine system has been implicated in the processing of social signals of offensive aggression in social-agonistic encounters in several species. In this study, we found that dopaminergic antagonism in healthy male volunteers, following acute administration of the dopamine D2-class receptor antagonist sulpiride, produced a selective disruption in the recognition of facial expressions of anger, signals of offensive aggression in humans. In contrast, recognition of other emotions and the matching of unfamiliar faces, were not significantly affected.