Cognitive neuroscience and disgust

Disgust is an emotion that is typically defined as an experience of a feeling of revulsion, that is sometimes accompanied by nausea along with several other physiological elements.^[1] Disgust may produce specific autonomic responses, such as reduced blood pressure, lowered heart-rate and decreased skin conductance along with changes in respiratory behaviour.^[2] A desire to withdrawal from the stimulus that elicits these feelings is also a key feature in the emotional feeling of disgust. Disgust is considered to be one of the six basic emotions confirmed by Paul Ekman, and is universal across cultures. It has only been recently that emotions have been recognized as a realm of cognitive neuroscience.^[3]

History

Evolutionary significance

It is believed that the emotion of disgust has evolved as a response to offensive foods that may cause harm to the organism.^[4] A common example of this is found in human beings who show disgust reactions to moldy milk or contaminated meat. Many researchers have claimed that the emotion of disgust functions to protect us from disease.^{[citation needed]} Disgust appears to be triggered by objects or people who possess particular types of features that signify disease.^[1]

Self-report and behavioural studies found that disgust elicitors include:

• body products (feces, urine, vomit, sexual fluids, saliva, and mucus);
• foods (spoiled foods);
• animals (fleas, ticks, lice, bugs, worms, flies, rats, and mice);
• hygiene (visible dirt and “inappropriate” acts [e.g., using an unsterilized surgical instrument]);
• body envelope violations (blood, gore, and mutilation);
• death (dead bodies and organic decay);
• visible signs of infection^[5]

The above-mentioned main disgust stimuli are similar to one another in the sense that they can all potentially transmit infections, and are the most common referenced elicitors of disgust cross-culturally.^[6]

Disgust recognition

In a series of significant studies by Paul Ekman in the 1970s, it was discovered that facial expressions of emotion are not culturally determined, but universal across human cultures and thus biological in origin.^[7] The facial expression of disgust was found to be one of these facial expressions. This characteristic facial expression includes slightly narrowed brows, a curled upper lip, wrinkling of the nose and visible protrusions of the tongue, although different elicitors may produce different forms of this expression.^[8] It was found that the facial expression of disgust is readily recognizable across cultures.^[9] This facial expression is also produced in blind individuals and is correctly interpreted by individuals born deaf.^[1] This evidence indicates an innate biological basis for the expression and recognition of disgust. The recognition of disgust is also important among species as it has been found that when an individual sees a conspecific looking disgusted after tasting a particular food, he or she automatically infers that the food is bad and should not be eaten.^[4] This evidence suggests that disgust is experienced and recognized almost universally and strongly implicates its evolutionary significance.

The mirror-neuron matching system found in monkeys and humans is a proposed explanation for such recognition, and shows that our internal representation of actions is triggered during the observation of another’s actions.^[10] It has been demonstrated that a similar mechanism may apply to emotions. Seeing someone else's facial emotional expressions triggers the neural activity that would relate to our own experience of the same emotion.^[11] This points to the universality, as well as survival value of the emotion of disgust.

The Neural Basis of Disgust

The scientific attempts to map specific emotions onto underlying neural substrates dates back to the first half of the 20th century. However, it was not until the mid-1990s when it was recognized that six basic emotions, including disgust, were each related to a specific neural structure and therefore considered to be a part of the clinical neurosciences.^[11]

Anterior Insula

The insula(or insular cortex), is the main neural structure involved in the emotion of disgust.^[4][11][12] The insula has been shown by several studies to be the main neural correlate of the feeling of disgust both in humans and in macaque monkeys. The insula is activated by unpleasant tastes, smells, and the visual recognition of disgust in conspecific organisms.^[4]

The anterior insula is an olfactory and gustatory center that controls visceral sensations and the related autonomic responses.^[4] It also receives visual information from the anterior portion of the ventral superior temporal cortex, where cells have been found to respond to the sight of faces.^[13]

The posterior insula is characterized by connections with auditory, somatosensory, and premotor areas, and is not related to the olfactory or gustatory modalities.^[4]

An In-Depth Look at Disgust in the Brain: Human Research

Several human studies have found that the insula is indeed important in the feeling and recognition of disgust in humans, including functional magnetic resonance imaging (f-MRI) and neuropsychological studies.

f-MRI Studies

In a study by Stark & colleagues (2007), sixty-six participants took part in an event-related fMRI analysis. 50 pictures were presented for four seconds and participants rated each picture on the dimensions disgust and fear. The results indicated that both fear and disgust stimulus categories resulted in activations in the occipital cortex, prefrontal cortex and in the amygdala.^[14] However, insula activation was only significantly correlated with ratings of disgust, pointing to a specific role of this brain structure in the processing of disgust. In another intensive fMRI study by Wicker & colleagues (2003), disgust reactions to visual and olfactory stimuli were compared. The study consisted of four runs and in the visual runs participants viewed movies of individuals smelling the contents of a glass (conditions: disgusting, pleasant, or neutral) and expressing the facial expressions of the respective emotions.^[4] In the olfactory runs, the same participants inhaled disgusting or pleasant odorants. It was found that the anterior insula was activated in both the observation of disgusted facial expressions (visual condition) and during the emotion of disgust evoked by unpleasant odors (olfactory condition).^[4] These findings demonstrate that observing someone else's facial expression of disgust seems to automatically retrieve a neural representation of disgust.^[4] Furthermore they emphasize the role of the insula in feelings of disgust across the senses.

Neuropsychological Studies

The fact that the insula is necessary for our ability to feel and recognize the emotion of disgust is further supported by neuropsychological studies. Both Calder (2000) and Adolphs (2003) showed that lesions on the anterior insula lead to deficits in the experience of disgust and recognizing facial expressions of disgust in others.^[12][15] The patients also reported having reduced sensations of disgust themselves. Furthermore, electrical stimulation of the anterior insula conducted during neurosurgery triggered nausea, the feeling of wanting to throw up and uneasiness in the stomach. Finally, electrically stimulating the anterior insula through implanted electrodes produced sensations in the throat and mouth that were “difficult to stand”.^[4] These findings demonstrate the role of the insula in transforming unpleasant sensory input into physiological reactions, and the associated feeling of disgust.^[4]

Animal Research

With respect to studies using rats, prior research of signs of a conditioned disgust response have been experimentally verified by Grill and Norgren (1978) who developed a systematic test to assess palatability. The Taste Reactivity (TR) test has thus become a standard tool in measuring disgust response.^[16] When given a stimulus intraorally which had been previously paired with a nausea-inducing substance, rats will show conditioned disgust reactions. “Gaping” in rats is the most dominant conditioned disgust reaction and the muscles used in this response mimic those used in species capable of vomiting.^[17] Recent studies have shown that treatments that reduced serotonin availability or that activate the endocannibinoid system can interfere with the expression of a conditioned disgust reaction in rats. These researchers showed that as nausea produced conditioned disgust reactions, by administering the rats with an antinausea treatment they could prevent toxin-induced conditioned disgust reactions. Furthermore, in looking at the different disgust and vomiting reactions between rats and shrews the authors showed that these reactions (particularly vomiting) play a crucial role in the associative processes that govern food selection across species.^[18] In discussing specific neural locations of disgust, research has shown that forebrain mechanisms are necessary for rats to acquire conditioned disgust for a specific emetic (vomit-inducing) substance (such as lithium chloride).^[19] Other studies have shown that lesions to the area postrema^[20] and the parabrachial nucleus of the pons^[21] but not the nucleus of the solitary tract^[21] prevented conditioned disgust. Moreover, lesions of the dorsal and medial raphe nuclei (depleting forebrain serotonin) prevented the establishment of lithium chloride-induced conditioned disgust.^[22]

Related Disorders

Huntington's Disease

It has been found that Huntington’s disease (a neurodegenerative disorder) can affect people’s recognition of disgust. One particular neuropsychological study focused on patient NK who was diagnosed a left hemisphere infarction involving the insula, internal capsule, putamen and globus pallidus. NK’s neural damage included the insula and putamen and it was found that NK’s overall response to disgust-inducing stimuli was significantly lower than that of controls.^[12] The patient showed a reduction in disgust-response on eight categories including food, animals, body products, envelope violation and death.^[12] Moreover, NK incorrectly categorized disgust facial expressions as anger. The results of this study support the idea that NK suffered damage to a system involved in recognizing social signals of disgust, due to a damaged insula caused by neurdegeneration.^[12] In another study of face perception and emotion recognition conducted by Sprengelmeyer & colleagues (1996), it was found that people with Huntington's disease were impaired at recognition of anger and fear, and experienced a notably severe problem with disgust recognition.^[23]

Obsessive-Compulsive Disorder

The emotion of disgust may have an important role in understanding the neurobiology of obsessive-compulsive disorder (OCD), particularly in those with contamination preoccupations.^[24] In a study by Shapira & colleagues (2003), eight OCD subjects with contamination preoccupations and eight healthy volunteers viewed pictures from the International Affective Picture System during f-MRI scans. OCD subjects showed significantly greater neural responses to disgust-invoking images, specifically in the right insula.^[25] Furthermore, Sprengelmeyer (1997) found that the brain activation associated with disgust included the insula and part of the gustatory cortex that processes unpleasant tastes and smells. OCD subjects and healthy volunteers showed activation patterns in response to disgust pictures that differed significantly at the right insula. In contrast, the two groups were similar in their response to threat-inducing pictures, with no significant group differences at any site.^[26]

Conclusion

Research in the past decade has led to an advanced understanding of basic emotions and the way in which they are organized within the brain. The advancements in neuroimaging technology have allowed researchers to make several new and developing findings.^[4] The research has supported that there are independent neural systems in the brain, each handling a specific basic emotion.^[4] Specifically, f-MRI studies have provided evidence for the activation of the insula in disgust recognition, as well as visceral changes in disgust reactions such as the feeling of nausea.^[4] The importance of disgust recognition and the visceral reaction of “feeling disgusted” is evident when considering the survival of organisms, and the evolutionary benefit of avoiding contamination.^[4]

See also

Cognitive neuroscience

Social neuroscience

Fear

Amygdala

Papez Circuit

Affective neuroscience

References

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