Emotion understanding

Up to now we have dealt with the neural mechanisms that enable individuals to understand "cold actions," that is, actions without any obvious emotional content. In social life, however, equally important, and maybe even more so, is the capacity to decipher emotions. Which mechanisms enable us to understand what others feel? Is there a mirror mechanism for emotions similar to that for cold action understanding?

It is reasonable to postulate that, as for action understanding, there are two basic mechanisms for emotion understanding that are conceptually different one from another. The first consists in cognitive elaboration of sensory aspects of others' emotional behaviors. The other consists in a direct mapping of sensory aspects of the observed emotional behavior on the motor structures that determine, in the observer, the experience of the observed emotion.

These two ways of recognizing emotions are experientially radically different. With the first, the observer understands the emotions expressed by others but does not feel them. He deduces them. A certain facial or body pattern means fear, another happiness, and that is it. No emotional involvement. Different is the case for sensory-motor mapping mechanism. In this case, the recognition occurs because the observed emotion triggers the feeling of the same emotion in the observing person. It is a first-person recognition. The emotion of the other penetrates the emotional life of the observer, evoking in him/her not only the observed emotion but also related emotional states and nuances of similar experiences.

As for cold action, our interest in this essay is the mechanisms underlying the direct sensory-motor mapping. For the sake of space, we will review data on one emotion only - disgust - for which rich empirical evidence has been recently acquired.

Disgust is a very basic emotion whose expression has an important survival values for the conspecifics. In its most basic, primitive form ("core disgust" Rozin et al. 2000) disgust indicates that something (e.g., food) that the individual tastes or smells is bad and, most likely, dangerous. Because of its strong communicative value, disgust is an ideal emotion for testing the direct mapping hypothesis.

Brain imaging studies showed that when an individual is exposed to disgusting odors or tastes, there is an intense activation of two structures: the amygdala and the insula (Augustine 1996; Royet et al. 2003; Small et al. 2003; Zald et al. 1998; Zald and Pardo 2000). The amygdala is a heterogeneous structure formed by several subnuclei. Functionally, these subnuclei form two major groups: the cor-ticomedial group and the basolateral group. The former, phylogenetically more ancient, is related to the olfactory modality. It is likely that it is the signal increase in the corticomedial group that is responsible for the amygdala activation in response to disgusting stimuli.

Similarly to the amygdala, the insula is a heterogeneous structure. Anatomical connections revealed two main functional subdivisions in it an anterior "visceral" sector and a multimodal posterior sector (Mesulam and Mufson 1982). The anterior sector receives a rich input from olfactory and gustatory centers. In addition, the anterior insula receives an important input from the inferotemporal lobe, where, in the monkey, neurons have been found that respond to the sight of faces (Gross et al. 1972; Tanaka 1996). Recent data demonstrated that the insula is the main cortical target of interoceptive afferents (Craig 2002). Thus, the insula is not only the primary cortical area for chemical exteroception (e.g., taste and olfaction) but also for the interoceptive state of the body ("body state representation").

The insula is not an exclusively sensory area. In both monkeys and humans, electrical stimulation of the insula produces body movements (Kaada et al. 1949; Penfield and Faulk 1955; Frontera 1956; Showers and Lauer 1961; Krolak-Salmon et al. 2003). These movements, unlike those evoked by stimulation of classical motor areas, are typically accompanied by autonomic and viscero-motor responses.

Functional imaging studies in humans showed that, as in the monkey, the anterior insula receives, in addition to olfactory and gustatory stimuli, higher order visual information. Observation of disgusted facial expressions produces signal increase in the anterior insula. (Phillips et al. 1997, 1998; Sprengelmeyer et al. 1998; Schienle et al, 2002).

Recently, Wicker et al. (2003) carried out an fMRI study in which they tested whether the same insula sites that show signal increase during the experience of disgust also show signal increase during the observation of facial expressions of disgust.

The study consisted of olfactory and visual runs. In the olfactory runs, individuals inhaled disgusting and pleasant odorants. In the visual runs, the same participants viewed video-clips of individuals smelling a glass containing disgusting, pleasant and neutral odorants and expressing their emotions.

Disgusting odorants produced, as expected, a very strong signal increase in the amygdala and in the insula, with a right prevalence. In the amygdala, activation was also observed with pleasant odorants, with a clear overlap between the activations obtained with disgusting and pleasant odorants. In the insula, pleasant odorants produced a relatively weak activation located in a posterior part of the right insula; disgusting odorants activated the anterior sector bilaterally. The results of visual runs showed signal increases in various cortical and subcortical centers but not in the amygdala. The insula (anterior part, left side) was activated only during the observation of disgust.

The most important result of the study was the demonstration that precisely the same sector within the anterior insula that was activated by the exposure to disgusting odorants was also activated by the observation of disgust in others (Fig. 3). These data strongly suggest that the insula contains neural populations that become active both when the participants experience disgust and when they see it in others.

The notion that the insula mediates both recognition and experience of disgust is supported by clinical studies showing that, following lesions of the insula, patients have a severe deficit in understanding disgust expressed by others (Calder et al. 2000; Adolphs et al. 2003). This deficit is accompanied by blunted and reduced sensation of disgust. In addition, electrophysiological studies showed that

Fig. 3. Illustration of the overlap (white) between the brain activation during the observation (blue) and the feeling (red) of disgust. The olfactory and visual analyses were performed separately as random-effect analyses. The results are superimposed on parasagittal slices of a standard MNI brain.

sites in the anterior insula, whose electrical stimulation produced unpleasant sensations in the patient's mouth and throat, are activated by the observation of a face expressing disgust.

Taken together, these data strongly suggest that humans understand disgust, and most likely other emotions (see Carr et al. 2003; Singer et al., 2004), through a direct mapping mechanism. The observation of emotionally laden actions activates those structures that give a first-person experience of the same actions. By means of this activation, a bridge is created between others and us.

The hypothesis that we perceive emotion in others by activating the same emotion in ourselves has been advanced by various authors (e.g., Phillips et al. 1997; Adolphs 2003: Damasio 2003a; Calder et al. 2000; Carr et al. 2003; Goldman and Sripada 2003; Gallese et al. 2004). Particulary influential in this respect has been the work by Damasio and his coworkers (Adolphs et al. 2000; Damasio 2003a, b) According to these authors, the neural basis of empathy is the activation of an "as-if-loop," the core structure of which is the insula (Damasio 2003). These authors attributed a role in the "as-if-loop" also to somatosensory areas like SI and SII, conceiving the basis of empathy to be in the activation in the observer of those cortical areas where the body is represented.

Although this hypothesis is certainly possible, the crucial role of the insula, rather than of the primary somatosensory cortices, in emotion feeling strongly suggests that the neural substrate for emotions is not merely sensorial. It is more likely that the activation of the insula representation of the viscero-motor activity is responsible for the first-person feeling of disgust. As for the premotor cortex, it is plausible that in the insula there is a specific type of mirror neurons that match the visual aspect of disgust with its viscero-motor aspects. The activation of these (hypothetical) viscero-motor mirror neurons should underlie the first-person knowledge of what it means to be disgusted. The activation of these insular neurons should not necessarily produce the overt viscero-motor response. The overt response should depend on the strength of the stimuli and other factors. A neurophysiological study of insula neuron properties could be the direct test of this hypothesis.

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