Elsevier

NeuroImage

Volume 34, Issue 4, 15 February 2007, Pages 1744-1753
NeuroImage

Empathy for positive and negative emotions in the gustatory cortex

https://doi.org/10.1016/j.neuroimage.2006.10.032Get rights and content

Abstract

Anterior insula and adjacent frontal operculum (hereafter referred to as IFO) are active during exposure to tastants/odorants (particularly disgusting ones), and during the viewing of disgusted facial expressions. Together with lesion data, the IFO has thus been proposed to be crucial in processing disgust-related stimuli. Here, we examined IFO involvement in the processing of other people’s gustatory emotions more generally by exposing participants to food-related disgusted, pleased and neutral facial expressions during functional magnetic resonance imaging (fMRI). We then exposed participants to pleasant, unpleasant and neutral tastants for the purpose of mapping their gustatory IFO. Finally, we associated participants’ self reported empathy (measured using the Interpersonal Reactivity Index, IRI) with their IFO activation during the witnessing of others’ gustatory emotions. We show that participants’ empathy scores were predictive of their gustatory IFO activation while witnessing both the pleased and disgusted facial expression of others. While the IFO has been implicated in the processing of negative emotions of others and empathy for negative experiences like pain, our finding extends this concept to empathy for intense positive feelings, and provides empirical support for the view that the IFO contributes to empathy by mapping the bodily feelings of others onto the internal bodily states of the observer, in agreement with the putative interoceptive function of the IFO.

Introduction

When we see the facial expressions of other individuals, we can often intuitively feel what they are feeling. The neural basis of this process has received intense interest. Based on the observations that the sight of other individuals’ actions activate similar action programs in the observer and that the observation of other individuals’ emotion of disgust activates regions of the brain involved in experiencing disgust, it has been proposed (Keysers et al., 2004, Gallese et al., 2004, Goldman and Sripada, 2005, Keysers and Gazzola, 2006) that feeling the emotions of other individuals involves the following: (a) observing the states of others activates representations of similar states in the observer; (b) these activations, which represent a form of simulation of the observed states, are sensed by a network of brain areas that represent bodily states; and (c) the sensed states are interpreted and attributed to the other individual, distinguishing them from the observer’s own emotions.

The distinction between these subprocesses relates to one made in psychology. Young babies, while witnessing the distress of other individuals, often cry as if they were unable to distinguish their own distress from that of others (for a review see Singer et al., 2006). This phenomenon has been termed ‘emotional contagion’. In contrast, while more mature individuals are not immune to emotional contagion, they are increasingly able to attribute the shared distress to the other individual, leading to an empathic understanding of the state of others (for reviews see Preston and de Waal, 2002, Gallese, 2003, Gallese et al., 2004, Decety and Jackson, 2004). Emotional understanding here refers to the conscious knowledge that someone else is currently experiencing a certain emotional state, as measured for instance by asking the observer to rate the emotional state of another individual (e.g. “how angry is that person from 0 to 6”, as used in Adolphs et al., 2003), or a forced choice labelling task, as used in Calder et al. (2000). The processes of simulating and sensing the simulated state of others, hypothesised earlier (Gallese et al., 2004, Keysers and Gazzola, 2006), would be common to emotional contagion and empathic understanding (for reviews see Critchley, 2005, Adolphs, 2006). Thus only the third process of attribution, that enables an observer to associate his/her own simulated emotional state to that of the observed, differentiates early emotional contagion from more mature empathic understanding (for reviews see Frith and Frith, 1999, Frith and Frith, 2003, Singer, 2006). According to that view (Gallese et al., 2004, Keysers and Gazzola, 2006), mirroring/resonance and/or contagion are important prerequisites for empathic understanding.

At present, the quest to provide empirical evidence for the simulation theory has focused on providing evidence for the fact that the brain creates a simulation of the states of other individuals, with current evidence suggesting that the observation of the negative states of others triggers neural activations that resemble those associated with experiencing similar negative states. Both the observation of disgusted facial expressions and the experience of disgust activate the anterior insula and the adjacent frontal operculum, which will jointly be referred to as IFO (Phillips et al., 1997, Zald et al., 2002, Small et al., 2003, Wicker et al., 2003, Dapretto et al., 2006). The IFO is also activated when participants observe facial expressions of pain, know a loved one is in pain or experience pain themselves (Singer et al., 2004, Singer et al., 2006, Decety and Jackson, 2004, Botvinick et al., 2005, Jackson et al., 2006, Lamm et al., in press, Saarela et al., in press), with the participants that report having more empathic concern activating their IFO more strongly while aware of others’ pain (Singer et al., 2004, Singer et al., 2006). In addition, lesions in the IFO impair both the experience of disgust (Adolphs et al., 2003) and the understanding of other people’s disgust (i.e. impaired labelling of facial and vocal expressions of disgust) (Calder et al., 2000, Adolphs et al., 2003). Together these experiments converge to ascribe a pivotal role for the IFO in the network of brain areas that underpin the process of simulating observed states of others making the insula a likely neural structure important both for emotional contagion and empathic understanding.

The IFO has also been identified as essential for sensing one’s own visceral bodily state (Craig et al., 2000, Critchley et al., 2001, Critchley et al., 2002, Critchley et al., 2003, Critchley et al., 2004, Critchley et al., 2005; for reviews see Damasio, 1996, Craig, 2002, Craig, 2003, Critchley, 2005), with people more able to sense their own heart beat showing stronger IFO responses (for a review see Critchley, 2005). Altogether, the IFO might therefore be engaged in two aspects that are key to simulation: the activation of simulated states, and the sensing of one’s own state, be it simulated or experienced (Keysers and Gazzola, 2006). In addition, the IFO has been shown to have the pattern of efferent and afferent connections necessary for performing both tasks (Mesulam and Mufson, 1982a, Mesulam and Mufson, 1982b, Mufson and Mesulam, 1982).

Is the IFO confined to the processing of negative states, such as pain and disgust, or does it also process positive states, as long as the latter are associated with the visceral sensations that the IFO is thought to represent? The ingestion of pleasant foods and liquids, associated with such positive bodily states, provide a way to test this prediction that has, to our knowledge, so far not been explored. We therefore scanned participants while they viewed short movie clips of actors sipping from a cup and displaying either an intensely pleased, intensely disgusted or a neutral facial expression. Subsequently, we then scanned the same participants while ingesting pleasant (sucrose), unpleasant (quinine) and neutral (artificial saliva) solutions to map their gustatory IFO.

Individuals differ in their sensitivity to the feeling states of others, and these differences can be measured using self-report questionnaires, such as the Interpersonal Reactivity Index (IRI, Davis, 1980). Here, we measured participants’ IRI scores and then searched for regions that respond more strongly to the gustatory experiences of others in participants with higher IRI scores. We restricted such a search to participants’ functionally defined gustatory IFO. As argued previously (Singer et al., 2004, Singer et al., 2006, Gazzola et al., 2006) this approach searches for areas underpinning our inter-individual variation in transforming the states of other people into our own, a process thought to be essential for emotional contagion and empathic sharing.

Section snippets

Participants and procedures

The institutional review board of the University Medical Center Groningen approved the study. Thirty-three healthy volunteers free from any known gustatory, olfactory, visual, neurological or psychiatric disorders gave written informed consent and participated in a screening and training sessions. Participants were screened for their taste sensitivity using labeled magnitude scaling (LMS) (Green et al., 1996), for the goal of excluding super/non tasters during the initial rating of the quinine

Ratings

In order to determine how much the emotional facial expressions in the movies affect the participants, we rated their subjective reaction to the gustatory emotions depicted in the films by asking how willing they would be to drink some of the beverage the individuals in the movies just tried (from − 6 ‘absolutely not willing’ to 6 ‘very much willing’); see Fig. 3. Furthermore, we asked them to rate the quinine, sucrose and neutral solutions that they had to ingest during the experiment on a

Discussion

Here, we examined whether the gustatory IFO activations during the vision of pleased and disgusted facial expressions correlated with how participants scored on a self report measure of their sensitivity to other people’s feeling states (IRI). We found that for both pleased and disgusted facial expressions, participants that obtained higher scores in the PD and FS subscales of the IRI activated their functionally defined gustatory IFO more strongly than participants obtaining lower scores. This

Acknowledgments

The authors thank the participants for their time, Anita Kuiper and Remco Renken for help in the acquisition of data, Dana Small for information on the chemosensory stimuli, Marina Maura and Johan van der Heiden for the preparation of the chemosensory stimuli, and Christian van der Gaag for the acquisition of the visual stimuli. We thank Tania Singer, Vittorio Gallese and John O’Doherty for their valuable comments. The research was supported by a Nederlandse Organisatie voor Wetenschappelijk

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