Hemodynamic brain correlates of disgust and fear ratings
Introduction
There is an ongoing debate which neural substrates are specific in the processing of the basic emotions fear and disgust and which have a more general role. The reviews by Calder et al. (2001) and Murphy et al. (2003) report that the insular cortex and the basal ganglia were more frequently activated during disgust processing than during fear processing while amygdala was more frequently activated in fear processing. This implicates that the neural mechanisms underlying disgust and fear might be separate in part. Murphy et al. (2003) and Phan et al. (2002) identified brain regions like the medial frontal cortex and the visual cortex responding to emotional stimuli in general.
Rolls (1999) assumes in his model that limbic structures – especially the amygdala – together with orbitofrontal areas are responsible for the evaluation of the reinforcement value of stimuli. Neural re-projections to primary and secondary sensory cortices ensure that salient stimuli are optimally processed (Amaral et al., 1993), resulting, in the case of visual stimuli, in increased neural activations in primary and secondary visual areas. Recent results of several fMRI studies in our research group using pictures of emotional scenes as stimuli in different experimental designs are in line with such integrative models of emotion. We were able to demonstrate that a set of different regions including the occipital–temporal cortex (OTC) and the amygdala are active during the processing of both fear and disgust (Schienle et al., 2002a, Schienle et al., 2005, Schienle et al., 2006, Stark et al., 2003, Stark et al., 2005).
However, the role of the insula within this network remains unclear. Schienle et al., 2005, Schienle et al., 2006 and Stark et al., 2003, Stark et al., 2004 found insula activation neither under fear-eliciting nor disgust-inducing stimulation, while Schienle et al. (2002a) and Schäfer et al. (2005) detected insula activation in both fear and disgust conditions. Mathews et al. (2004) found increased activation in both insula and amygdala in response to fear-related vs. neutral pictures. In contrast, Wright et al. (2004), using pictures of disgusting scenes, reported insula activation to be disgust-specific.
Some of these inconsistencies, we hypothesize, could be due to inter-individual differences in the experience of emotional stimuli. Most of the fMRI studies mentioned above used block designs, i.e. the emotional stimuli were presented in homogenous blocks of the same category (e.g. Schienle et al., 2006, Wright et al., 2004). The brain activation towards highly intense emotional stimuli is thereby contrasted with the activation towards blocks of neutral stimuli. Such an approach does not consider individual differences in the reactions to the emotional stimuli, even if participants have to rate the stimuli after the experiment. These post hoc ratings are usually not included into the statistical model but only used to verify the a priori assigned emotional categories. Post hoc ratings can further be problematic because they are subject to memory and habituation effects. Therefore, it seems appropriate to rate the stimuli immediately after each presentation. Individual ratings can then be entered into the statistical analyses instead of using a priori assignments.
Heinzel et al. (2005) followed this approach using visual emotional stimulation with pictures of emotional scenes. They showed that functional activations in the orbitofrontal and dorsomedial prefrontal cortex, as well as in the medial parietal cortex and the insula were significantly correlated with the subjective ratings of emotional valence (ranging from positive to negative). Anders et al. (2004) investigated the relationship between different emotional response systems (subjective ratings, electrodermal responses, startle reflex) and functional brain activation in a picture perception paradigm. Starting from the two dimensions of the verbal emotional space, valence (positive vs. negative) and arousal (high vs. low), they found that subjective ratings of negative valence (“unpleasant”) correlated with the activation of the insula. The arousal ratings of the pictures were significantly related to thalamic activation. Yet, these studies did not aim at a comparison of specific emotions but used emotion unspecific dimensions like valence or arousal for correlation with the fMRI data.
In the present study we directly compared the neural correlates of the basic emotions fear and disgust in an event-related picture perception paradigm. That is, we did not present the pictures in homogenous blocks of the same emotional category and intensity but in single trials with a randomized order of pictures. These pictures covered a broad range of emotional intensities. We measured the subjective ratings in this parametric design online, directly after each picture presentation. We presumed that the inclusion of the subjective ratings into the statistical analyses would help to improve the detection of possible differences and similarities in fear- and disgust-related brain activations. The study also allowed comparing the results of this parametric approach with those of a classical categorical fear vs. disgust contrast.
Section snippets
Participants
Sixty-six healthy right-handed participants took part in the study (34 males, 32 females). They were 19 to 44 years old (mean age: 24.7 years, SD = 5.2) and most of them were students, who received either course credits or were paid (15 Euros) for their participation. None of them was taking regular medication or had a previous history of psychiatric or neurological treatment. The study was performed in accordance with the ethical standards established in the fifth revision of the Declaration of
Subjective ratings, skin conductance, and viewing time
The analyses of variance revealed significant differences between the picture categories in all variables (all F-values > 6). As expected, the fear- and disgust-inducing pictures were rated as more negative in valence (FEAR-NEUTRAL, valence: D = 2.87, SE = 0.14, p < 0.001; DISGUST-NEUTRAL, valence: D = 2.69, SE = 0.14, p < 0.001) and more arousing (FEAR-NEUTRAL, arousal: D = 3.41, SE = 0.16, p < 0.001; DISGUST-NEUTRAL, arousal: D = 1.99, SE = 0.14, p < 0.001) than the neutral pictures. They were also rated as more fear-
Discussion
The present study investigated the neural correlates of fear and disgust using event-related fMRI in a parametric statistical design that considered each participant's individual evaluation of the stimuli with regard to feelings of disgust and fear.
Both fear and disgust ratings correlated with the activation of occipito-temporal regions,1
Acknowledgments
This research was supported by a grant to R. Stark from the German Research Society (Az. STA 475/4-1).
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