Simulation theory of empathy

Simulation theory of empathy

The simulation theory of empathy put forward by Rutgers philosopher Alvin Goldman attempts to explain how humans understand others' emotions and sensations. It posits that the perception of others’ experiences activates shared neural networks in the observers so that people can implicitly experience the emotions and sensations of the observed target. [Preston, S.D., & de Wall, F.B.M. (2002). Empathy: its ultimate and proximate bases. Behavioral and Brain Sciences, 25, 1-72.] [Decety, J., & Jackson, P.L. (2004). The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews, 3, 71-100.] For example, people feel disgust when they see others smell bad odor, [ Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003) Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron, 40(3), 655-664.] they feel pain when they see others being pierced by a needle or get electrical shock, [Avenanti, A., Paluello, L. M., Bufalari, I., & Aglioti, S. M. (2006). Stimulus-driven modulation of motor-evoked potentials during observation of others' pain. Neuroimage, 32(1), 316-324] they sense touching when they see others being brushed, [Keysers, C., Wicker, B., Gazzola, V., Anton, J. L., Fogassi, L., & Gallese, V. (2004). A touching sight: SII/PV activation during the observation and experience of touch. Neuron, 42(2), 335-346.] and they feel sad when they see others’ sad facial expressions. [ Harrison, N. A., Singer, T., Rotshtein, P., Dolan, R. J., & Critchley, H. D. (2006). Pupillary contagion: Central mechanisms engaged in sadness processing. SCAN, 1, 5-17 ]

Origin

The simulation theory of empathy is actually based in philosophy of mind, especially the work of Alvin Goldman and Robert Gordon. Then, the discovery of mirror neurons in macaque monkeys has provided a physiological mechanism for the common coding betwee perception action (see Wolfgang Prinz) [di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events - A neurophysiological study. Experimental Brain Research, 91(1), 176-180] and the hypothesis of a similar mirror neuron system in the human brain. [Preston, S.D., & de Wall, F.B.M. (2002). Empathy: its ultimate and proximate bases. Behavioral and Brain Sciences, 25, 1-72.] [ Iacoboni, M., Woods, R. P., Brass, M., Bekkering, H., Mazziotta, J. C., & Rizzolatti, G. (1999). Cortical mechanisms of human imitation. Science, 286(5449), 2526-2528 ] Since the discovery of the mirror neuron system, many studies have been carried out to examine the role of this system in action understanding, emotion and other social functions.

Development

Mirror neurons are activated both when actions are executed and the actions are observed. This unique function of mirror neurons may explain how people recognize and understand the states of others; mirroring observed action in the brain as if they conducted the observed action [Gallese, V., Keysers, C., & Rizzolatti, G. (2004). A unifying view of the basis of social cognition. Trends in Cognitive Sciences, 8(9), 396-403 ] .

Two sets of evidence suggest that mirror neurons in the monkey have a role in action understanding. First, the activation of mirror neurons requires biological effectors such as hand or mouth. Mirror neurons do not respond to the action with tools like pliers. [ Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593-609 ] Mirror neurons respond to neither the sight of an object alone nor an action without an object (intransitive action). Umilta and colleagues [ Umilta, M. A., Kohler, E., Gallese, V., Fogassi, L., Fadiga, L., Keysers, C., et al. (2001). I know what you are doing: A neurophysiological study. Neuron, 31(1), 155-165] demonstrated that a subset of mirror neurons fired when final critical part of the action was not visible to the observer. The experimenter showed his hand moving toward a cube and grasping it, and later showed the same action without showing later part grasping the cube (placing the cube behind the occluder). Mirror neurons fired on both visible and invisible conditions. On the other hand, mirror neurons did not discharge when the observer knew that there was not a cube behind the occluder.

Second, responses of mirror neurons to same actions are different depending on context of the action. A single cell recording experiment with monkeys demonstrated the different level of activation of mouth mirror neurons when monkey observed mouth movement depending on context (ingestive actions such as sucking juice vs. communicative actions such as lip-smacking or tongue protrusions). [ Ferrari, P. F., Gallese, V., Rizzolatti, G., & Fogassi, L. (2003). Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. European Journal of Neuroscience, 17(8), 1703-1714] An fMRI study also showed that mirror neurons respond to the action of grasping a cup differently depending on context (to drink a cup of coffee vs. to clean a table on which a cup was placed). [Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J. C., & Rizzolatti, G. (2005). Grasping the intentions of others with one's own mirror neuron system. Plos Biology, 3(3), 529-535 ]

Emotion understanding

Shared neural representation for a motor behavior and its observation has been extended into the domains of feelings and emotions. Not only movements but also facial expressions activate the same brain regions that are activated by direct experiences. In an fMRI study, same brain regions on action representation found to be activated when people both imitated and observed emotional facial expressions such as happy, sad, angry, surprise, disgust, and afraid. [Carr, L., Iacoboni, M., Dubeau, M. C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences of the United States of America, 100(9), 5497-5502 ] .

Observing video clips that displayed facial expression of feeling disgust activated the neural networks typical of direct experience of disgust. [Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron, 40(3), 655-664 ] . Similar results have been found in the case of touch. Watching movies that someone touched legs or faces activated the somatosensory cortex for direct feeling of the touch. [ Keysers, C., Wicker, B., Gazzola, V., Anton, J. L., Fogassi, L., & Gallese, V. (2004). A touching sight: SII/PV activation during the observation and experience of touch. Neuron, 42(2), 335-346 ] A similar mirror system exists in perceiving pain. When people see other people feel pain, people feel pain not only affectively, [ Avenanti, A., Paluello, L. M., Bufalari, I., & Aglioti, S. M. (2006). Stimulus-driven modulation of motor-evoked potentials during observation of others' pain. Neuroimage, 32(1), 316-324.] but also sensorially. [ Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303(5661), 1157-1162]

These results suggest that understanding other's feelings and emotions is driven not by cognitive deduction of what the stimuli means but by automatic activation of somatosensory neurons. A recent study on pupil size directly demonstrated emotion perception was automatic process modulated by mirror systems. [ Harrison, N. A., Singer, T., Rotshtein, P., Dolan, R. J., & Critchley, H. D. (2006). Pupillary contagion: Central mechanisms engaged in sadness processing. SCAN, 1, 5-17] When people saw sad faces, pupil sizes influenced viewers in perceiving and judging emotional states without explicit awareness of differences of pupil size. When pupil size was 180% of original size, people perceived a sad face as less negative and less intense than when pupil was smaller than or equal to original pupil size. This mechanism was correlated with brain regions that implicated in emotion process, the amygdala. Furthermore, viewers mimic the size of their own pupils to those of sad faces they watched. Considering that pupil size is beyond voluntary control, the change of pupil size upon emotion judgment is a good indication that understanding emotions is automatic process. However, the study could not find other emotional faces such as happiness and anger influence pupil size as sadness did.


= Epistemological role of empathy =

Understanding other’s actions and emotions is believed to facilitate efficient human communication. Based on findings from neuroimaging studies, de Vignemont and Singer [ de Vignemont, F., & Singer, T. (2006). The empathic brain: How, when and why? Trends in Cognitive Sciences, 10(10), 435-441] proposed empathy as a crucial factor in human communication arguing its epistemological role; “Empathy might enable us to make faster and more accurate predictions of other people’s needs and actions and discover salient aspects of our environment.” Mental mirroring of actions and emotions may enable humans to understand other’s actions and their related environment quickly, and thus help humans communicate efficiently [ Gallese, V., Keysers, C., & Rizzolatti, G. (2004). A unifying view of the basis of social cognition. Trends in Cognitive Sciences, 8(9), 396-403 ] .

In an fMRI study, a mirror system has been proposed as common neural substrates to mediate the experiences of basic emotions [ Chakrabarti, B., Bullmore, E., & Baron-Cohen, S. (2006). Empathizing with basic emotions: Common and discrete neural substrates Social Neuroscience, 1(3&4), 364-384] . Participants watched video clips of happy, sad, angry and disgust facial expressions, and measured their Empathy Quotient (EQ). Specific brain regions relevant to the four emotions were found to be correlated with the EQ while the mirror system (i.e., the left dorsal inferior frontal gyrus/premotor cortex) was correlated to the EQ across all emotions. The authors interpreted this result as an evidence that action perception mediates face perception to emotion perception.

Empathy for pain

A paper published in Science (Singer et al., 2005) [Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303(5661), 1157-1162] challenges the idea that pain sensations and mirror neurons play a role in empathy for pain. Specifically, the authors found that activity in the anterior insula and he anterior cingulate cortex was present both when one's self and another person were presented with a painful stimulus, two regions known to be responsible for the affective experience of pain, but the rest of the pain matrix, responsible for sensation, was not active. Furthermore, participants merely saw the hand of another person with the electrode on it, making it unlikely that 'mirroring' could have caused the empathic response. However, a number of other studies, using magnetoencephalography and functional MRI have since demonstrated that empathy for pain does involve the somatosensory cortex, which supports the simulation theory. [Cheng, Y., Yang, C.Y., Lin, C.P., Lee, P.R., & Decety, J. (2008). The perception of pain in others suppresses somatosensory oscillations: a magnetoencephalography study. NeuroImage, 40, 1833-1840.] [Moriguchi, Y., Decety, J., Ohnishi, T., Maeda, M., Matsuda, H., & Komaki, G. (2007). Empathy and judging other’s pain: An fMRI study of alexithymia. Cerebral Cortex, 17, 2223-2234.] [Lamm, C., Nusbaum, H.C., Meltzoff, A.N., & Decety, J. (2007). What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLoS ONE, 12, e1292.] [Ogino, Y., Nemoto, H., Inui, K., Saito, S., Kakigi, R., & Goto, F. (2007). Inner experience of pain: imagination of pain while viewing images showing painful events forms subjective pain representation in human brain. Cerebral Cortex, 17, 1139-1146.]

Support for anterior insula and anterior cingulate cortex being the neural substrates of empathy include Wicker et al., 2003 who report that their "core finding is that the anterior insula is activated both during observation of disgusted facial expressions and during the emotion of disgust evoked by unpleasant odorants" [Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003) Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron, 40(3), 655-664.] (p. 655).

Furthermore, one study demonstrated that "for actions, emotions, and sensations both animate and inanimate touch activates our inner representation of touch." They note, however that "it is important at this point to clarify the fact that we do not believe that the activation we observe evolved in order to empathize with other objects or human beings" [Keysers, C., Wicker, B., Gazzola, V., Anton, J. L., Fogassi, L., & Gallese, V. (2004). A touching sight: SII/PV activation during the observation and experience of touch. Neuron, 42(2), 335-346] (p. 343).

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