b Amygdala and fear processing a functional imaging perspective

Imaging teclmiques such as fMRI and PET have also examined the brain processes involved in fear perception. The amygdala shows more activity in response to facial displays of fear when compared to responses to neutral faces, (Breiter et al., 1996; Hariri, Bookheimer, & Mazziotta, 2000; Phillips, Young et al., 1998; Phillips et al., 1997; Sprengelmeyer, Rausch, Eysel, & Przuntek, 1998). Elevated amygdala activity is associated with fearful faces and voices in comparison with disgust faces (Phillips, Young et al., 1998; Phillips et al., 1997) and in comparison with happiness facial stimuli (Morris, Friston et al., 1998; Morris et al., 1996; Whalen et al., 1998). From a number of studies, Calder and co-workers (2001) summarised the maximally activated voxels involving the amygdala in response to the presentation of fear faces. They reported a propensity for left amygdala activity in response to facial expressions, while fearful displays engage the amygdala bilaterally. Fearful facial displays especially involve dorsal amygdala activity. Phelps and co-workers (2001) manipulated experimental conditions, so that participants thought that they would receive a shock (threat) when a particular coloured square was presented. In this condition, skin conductance levels changed and there was significant activity within the left amygdala.

LeDoux (1989) proposed a fear reaction system, in which threat signals are transmitted from the thalamus to the amygdala (fast subcortical route) and from the sensory cortex to the amygdala (the cortical route). Indeed, support for the subcortical route has come from numerous studies (DeGelder, Vroomen, Pourtois, & Weiskrantz, 1999; Moms, DeGelder, Weiskrantz, & Dolan, 2001; Morris, Ohman, & Dolan, 1998, 1999). These studies suggest that cortical blindness or lack of conscious awareness of threat-related stimuli do not prevent activity in the amygdala in response to the visual presentation of fearful faces. In contrast, Phillips and collaborators (2004) demonstrated that overt presentation of fear stimuli (170ms) is cmcial to activating the amygdala, yet short presentation (30ms) is insufficient to trigger responses of this structure.

Imaging studies have supplemented neuropsychological research, providing evidence for amygdala involvement in cross-modal fear perception, since facial and vocal expressions of fear activated the amygdala and superior temporal gyrus (Phillips,

Young et al., 1998). Morris and colleagues (1999) reported a decreased response in the amygdala and left anterior insula for fearful voices in comparison to sad, happy, and neutral voices. Thus, while the type of response differs, the amygdala is associated with listening to fearful voices in both of these studies.

1.5.2c Neural substrate for fear processing - a summary

In summary, neuropsychological studies of people with damage to the amygdala have indicated that this structure plays some role in fear recognition, since these people have difficulty recognising fear displayed by others and to a lesser extent, experiencing it themselves (Adolphs et al., 1994; Adolphs et al., 1995; Adolphs et al., 1999; Broks et al., 1998; Calder et al., 2001; Scott et al., 1997; Sprengelmeyer et al., 1999; Wang et al., 2002). Functional imaging research has supported this, by showing that the amygdala is activated when participants are exposed to threat-related stimuli (Morris, Friston et al., 1998; Morris et al., 1996; Morris, Ohman et al., 1999; Morris, Scott et al., 1999; Phillips et al., 1999; Phillips, Young et al, 1998; Sprengelmeyer et al, 1998). Please see Sections 1.5.3a-1.5.3b for discussion of the shortcomings of the amygdala theory.

1.5.2d Basal ganglia, insula cortex, and disgust processing - a neuropsychological

perspective

There is strong evidence for the involvement of the insula cortex and basal ganglia in emotion processing. Their role is not clear, but research has posited that these regions are related to understanding and expressing emotions (Cancelliere & Kertesz, 1990). The basal ganglia are a collection of nuclei, which include the striatum (the caudate nucleus, putamen, nucleus accumbens), global pallidus, substantia nigra and the subthalamic nucleus (see Figures 1.3 and 1.4).

caudate S t putamen globus pallidus thalamus subthalamic nucleus substantia nigra

Figure 1.3: The connections o f the basal ganglia.

p.c. - substantia nigra pars compacta, p.r. - substantia nigra pars reticulata. .Source: http://thalamus, wustl.edu/course/

Figure 1.4: The basal ganglia.

I. Corona radiata. 2. Corpus callosum. 3. Head o f caudate nucleus. 4. Body o f caudate nucleus. S. Tail o f caudate nucleus. 6. "Foot" o f lentiform nucleus. 7. .Amygdaloid nuclear complex 8. Optic tract V. Putamen. 10. Bridges o f grey matter between putamen and caudate nucleus 11. Pulvinar o f thalamus. 12. Bulb o f occipital horn o f lateral ventricle. 13. Calcar avis. 14. Collateral trigone. 15. Collateral eminence. 16. Hippocampus. 17. Inferior longitudinal fasciculus. 18. Short arcuate fibers

Source: http://www.vh.org/Providcrs/Textboo/cs/BrainAnatomy/Braift4natomy.html

Double dissociations in neuropsychological research provide further support for the hypothesis that there are independent mechanisms underlying the processing o f specific emotions. In contrast to fear research, the emotion o f disgust has been associated with a distinctly different neural correlate. Huntington’s disease is a severe neurogenetic disorder, characterised by late-on set degeneration o f the striatum. Patients suffering from H untington’s disease experience impaired recognition o f facial expressions o f disgust in comparison to other facial expressions o f emotion

(Sprengelmeyer et al., 1996; Sprengelmeyer, Young, Sprengelmeyer et al., 1997; Wang, Hoosain, Yang, Meng, & Wang, 2003). Fear perception remains relatively intact, thus a double dissociation between fear and disgust processing has been claimed. The same facial tasks administered to amygdala patients (Broks et al., 1998; Calder, Young, Rowland et al., 1996; Sprengelmeyer et al., 1999) were used in these experiments. Sprengelmeyer and colleagues (1996) also reported that Huntington’s patients had abnormal performance in a task assessing disgust recognition from vocal cues. Moreover, the presence of the gene mutation responsible for the development of Huntington’s disease leads to problems in perceiving facial disgust, even when the symptoms of this illness are not present (Gray, Young, Barker, Curtis, & Gibson,

1997). A degree of basal ganglia degeneration is associated with this state. These studies provide neuropsychological evidence for some role of the basal ganglia in disgust processing.

Abnormal metabolic activity within the basal ganglia is observed in cases of Obsessive-Compulsive Disorder (OCD) and Tourette’s syndrome (Braun et al., 1995; Rapoport, 1989; Rapoport & Fiske, 1998). OCD is a complex, heterogeneous anxiety disorder, defined by presence of either self-recognised irrational or unreasonable obsessions or compulsions, which affect everyday functioning. Tourette’s syndrome is a tic disorder that is characterised by early onset and social or occupational functioning impairment and often includes OCD-type behaviours (APA, 1994; Braun et al., 1995). Interpretation of facial displays of disgust is also disturbed in OCD and Tourette’s, but only if OCD symptoms are detected in its diagnosis (Sprengelmeyer, Young, Pundt et al., 1997). Sprengelmeyer and colleagues suggested that the presence of obsessive-compulsive behaviours is a defining feature of the disgust deficit.

Dysfunction in regions of the basal ganglia, particularly the striatum and the substantia nigia, also occurs in Parkinson’s disease. Consequently, research has focused on whether there are interferences in the processing of disgust stimuli in patients with this disease. Unmedicated Parkinson’s patients were significantly worse at perceiving facial disgust than their medicated counteiparts and a control gioup (Sprengelmeyer et al., 2003). This disgust deficit, specific to faces, has been reported in another study (Kan, Kawamura, Hasegawa, Mochizuki, & Nakamura, 2002). Facial and vocal fear recognition accuracy combined is impaired in Parkinson’s

patients with bilateral Parkinson’s disease (Yip, Lee, Ho, Tsang, & Li, 2003). Yet groups with Parkinson’s symptoms exhibited on their right side were less accurate at perceiving disgust and sadness from the facial and vocal channels pooled together. Disgust is believed to have evolved in order prevent us from ingesting hannful substances and to communicate this danger to others (Rozin, Haidt, & McCauley, 2000). Thus, one would expect this emotion to involve multiple sensory inputs. In a neuropsychological case study, an individual with insula cortex and putamen damage had gieat difficulty recognising disgust from faces and from voices, both from non­ verbal cues and prosodic cues (Calder, Keane, Manes, Antoun, & Young, 2000). Yet he understood what was meant by disgust. Thus, the concept and recognition do not seem to be related. The basal ganglia and insula are highly interconnected. Adolphs and colleagues (2003) also examined a participant with extensive neural damage, particularly to the insula cortex, and found him to have profound difficulties in perceiving disgust from dynamic facial expressions and emotional descriptions, and he seemed to have an abnormal experience of this emotion. These two studies imply that when the insula-striatal system is compromised, disgust processing is impaired, thus indicating a role for this system in disgust processing. It is also important to note that an abnormal increase in activation of insula in response to sensory processing and movement processing is also associated with Huntington’s disease (Boecker et al., 1999; Weeks et al., 1997). Thus, the insula cortex would be a suitable candidate for processing disgust. It has also been labelled as the gustatory cortex since it contains neurons that respond to pleasant and unpleasant tastes (Small et al., 1999; Yaxley, Rolls, & Sienkiewicz, 1988). This is fitting, given the proposed phylogenetic origins of disgust as a rejection response to bad tastes (Rozin et al., 2000). Therefore, disgust seems to be linked with gustation and the insula cortex. There are studies that conflict with the proposal that disgust is processed by a separable neural mechanism, however. Please see Sections 1.5.3c-1.5.3d.

1.5.2e Basal ganglia, insula cortex, and disgust processing - afunctional imaging

perspective

Functional imaging studies have been particularly informative because the brain regions involved in disgust are not clear; Huntington’s and Parkinson’s disease, and

OCD are not associated with overlapping or selective neural degeneration. fMRI was used to compare neural activity when participants viewed neutral and disgusted faces. Strong and mild expressions of disgust activated the insula and basal ganglia nuclei (Phillips et al., 1997). The amygdala was not activated by disgust. This provides a further evidence for separable structures involved in fear and disgust processing. Extensions of this work revealed that the anterior insula, the caudate, and putamen were involved in facial disgust perception (Phillips, Young et al., 1998; Sprengelmeyer et al., 1998). Recordings of intracerebral event-related potentials further revealed the importance of the ventral anterior insula in the perception of facial expressions, particularly those representing disgust (Krolak-Salmon et al., 2003).

A recent fMRI exploration has examined the neural activity of a group of pre- symptomatic Huntington’s disease gene-carriers when disgusted faces were exhibited (Hennenlotter et al., 2004). Gene caiTiers had reduced responses within the left dorsal anterior insula in response to disgusted but not surprised or neutral faces, which in control participants showed an increase in activation. Behaviourally, the gene carriers were impaired in perceiving disgust. This study provides additional evidence for the role of the insula cortex in the processing of disgust.

Furthermore, disgusting pictures also seem to activate the insula cortex (Phillips et al., 2000). Heining (2003) found that the insula responded to the presentation of disgust in auditory, gustatory, visual, and olfactory channels. This suggests that there may be some sort of multi-modal system for processing disgust, which involves regions of the insula and basal ganglia. Various research contests this idea, however. Please see Section 1.5.3c.

l,5 ,2 f Neural substrate for disgust processing - a summary

In summary, disgust has been associated to neural structures including the insula cortex and the basal ganglia, but not the amygdala. Neuropsychological studies have provided strong support for the role of the basal ganglia and insula cortex in disgust processing (Adolphs et al., 2003; Calder, Keane, Manes et al., 2000; Gray et al., 1997;

sprengelmeyer et al., 1996; Sprengelmeyer, Young, Pundt et al, 1997; Wang et al, 2003).

The studies presented in Section 1.5.2e support the neuropsychological proposal that processing facial disgust may be separable from fear processing; and that disgust perception may rely on the insula or basal ganglia (Hennenlotter et al, 2004; Phillips et al, 2000; Phillips, Senior, Fahy, & David, 1998; Phillips, Young et al, 1998; Phillips et al, 1997; Sprengelmeyer et al, 1998).

1.5.3 A case for questions against independent neural pathways for specific