Tania Singer Social Cognitive Neuroscience and the Example of Empathy Wellcome Department of Imaging Neuroscience UCL Institute of Cognitive Neuroscience University College of London

Topics in Social-Cognitive Neuroscience How do we process and represent other people’s minds and how do they influence us? Perception and memory of socially salient features (i.e. facial attractiveness, trustworthiness, emotional expressions) Action observation (Imitation, mirror neurons) Theory of Mind (TOM) & Mentalizing Empathy Moral emotions and moral and social reasoning Self Concept, Distinction between Self and Others Social Level Behavioral Level Cognitive Level Neural Level (e.g. facial expressions of emotions, attractiveness or trustworthiness, racial identity of faces, biological motions, eye gaze, odours, vocal cues)

Emotional Facial Expressions Familiar and Famous Faces Perception of Socially Salient Features Emotional Facial Expressions Familiar and Famous Faces Morris et al. (1986). Nature; Phillips et al., (1997). Nature.

Social Rewards: Attractive Faces Mildly Happy Neutral O’Doherty et al. (2003). Neuropsychologia

Social Judgement: Trustworthiness of Faces Task Face Trustworthy Untrustworthy Judge age ‘Implicit task’ Judge trustworthiness ‘Explicit task’ Parametric scale based on subjects own ratings We designed an experiment in which Brothers’ model could be tested. We presented 120 greyscale Caucasian male faces to 14 subjects whilst they underwent functional MRI scans. Faces depicted either school or university age students. The minimum stimulus onset asynchrony was 3s, and 60 null events were interspersed with the faces, which were presented for one second each. During scanning, subjects viewed half the faces and made a judgement of whether the face was that of a school-boy or university student and made a binary trustworthiness judgement on the other half of the faces. The order of these tasks was counterbalanced across subjects. Following scanning, subjects viewed all faces again and provided a rating of trustworthiness for each face on a scale from 1-7. fMRI data were analysed using SPM99 employing an event-related model and random effects statistics for population level inference. Note that although the slide depicts the experimental design as 2X2, the factor of trustworthiness was in fact analysed parametrically in our analysis. This allowed us to find regions showing responses that increased or decreased with perceived trustworthiness of the face. A great strength of this design is the use of the participants’ own ratings of the faces in the subsequent statistical analysis. An independent, age-matched group of subjects additionally rated the faces for four basic emotions - anger, fear, happiness and sadness. These data were used to explore the potential confounds of facial expression on trustworthiness. Winston et al. (2002). Nature Neuroscience

Socially Salient Cues of the Body: Biological Motion

Brothers’ Extended Model of Social Cognition General Findings Brothers’ Extended Model of Social Cognition Insula/somato- sensory cortices STS Striatum OFC Fusiform Amygdala

Adolphs Model of Social Cognition (2003) Detailed perceptual processing Fusiform gyrus Superior temporal gyrus Motivational Evaluation Amygdala Orbito-frontal cortex Ventral striatum Emotional Response in body autonomic, visceral endocrine change Representation of emotion response Insula-somatosensory cortices Adolphs, R. (2003). Cognitive Neuroscience of Human Social Behavior. Nature Neuroscience Reviews

The Amygdala and its Modulatory Role

Social-Cognitive Neuroscience Social Neuroscience provides insights into people’s ability to understand the mental states and share the feelings of others. Three Streams of Research in Social Neuroscience ● Theory of Mind (TOM) & Mentalizing ● Action Observation, Imitation (Mirror Neurons) ● Empathy (e.g. facial expressions of emotions, attractiveness or trustworthiness, racial identity of faces, biological motions, eye gaze, odours, vocal cues)

Modern Social Neuroscience: How do we Understand the Other ? Theory of Mind (TOM) & Mentalizing refers to our ability to understand mental states such as intentions, desires and believes of others. Empathy refers to our ability to share the feelings of others, be it a particular emotion or sensory state of the other. (e.g. facial expressions of emotions, attractiveness or trustworthiness, racial identity of faces, biological motions, eye gaze, odours, vocal cues)

A Paradigm to Measure Empathy ‚In Vivo‘ Using the Example of Pain The ‘Pain Matrix’ in the Brain Singer et al. (2004). Science

Shared Networks for Pain in Self and Others Y = 12 x = - 6 Bilateral anterior insula ACC -0.2 -0.1 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 10 15 20 25 Anterior Cingulate [-9, 6, 39] r = 0.62 Empathy Scores Left Anterior Insula [-33, 9, 6] r = 0.52

Recent fMRI Studies on Empathy for Pain Singer et al. (2004). Y = 12 ACC Bilateral anterior insula Morrison et al. (in 2004). Seeing pictures of body parts in painful situations Singer et al. (2006). Nature Seeing facial expressions of Pain 6 Jackson, Metzoff & Decety (2004). NeuroImage. Botvinick et al. (in press).

fMRI Studies on Emotional Contagion Wicker et al., 2003. Both the observation of disgusted faces and smelling disgusting odours activated the same restricted group of brain structures, including the insula and ACC. Keysers et al., 2004. Secondary but not the primary somatosensory cortex is activated when the participants were touched and when they observed someone or something else getting touched by objects. but see Blakemore et al., 2005

Conclusion When empathizing with others’ affective states we activate representations reflecting the same bodily states in ourselves. These shared affective representations allow us to know how it feels like for someone else to be for example in pain even in the absence of any stimulation to our own body

Modulation of Empathic Responses Theories of social preferences predict that empathy should be modulated by the perceived fairness of other individuals, and that individual agents punish violations of social norms. Thus, empathy should be reduced or abolished towards agents whose behaviour deemed socially unfair and thus whom we dislike. Instead we might expect to observe evidence of ‘Schadenfreude’ – the feeling of satisfaction experienced when social violators experience punishment –as predicted by studies of altruistic punishment

The Experimental Paradigm Stage 1: Social learning Subjects play repeated prisoners dilemma with 2 opponents – one fair, the other unfair Stage 2: Empathy for Pain Paradigm Subjects observe both players in an in-vivo empathy for pain study Singer et al. (2004). Neuron Singer et al. (2006). Nature

One Game of the Social Learning Phase Investment Waiting Yes No You have 10 Points Do you want to send your money? Decision This is your playing partner Pay-off Your points 30 Your partners points 3 sec. Wait for her decision Prepare for the next game 3-12 sec. Your Partner decided to send You 10 points 3-6 sec. 3 sec. Time Course of one Game 3 sec.

The Actors and the Experimental Setting

Ratings for Fair and Unfair Partner as a Function of Gender -2 -1 1 2 fair/ reason. pleasant/ agreeable attractive sorry like Female Fair Confederate Female Unfair Confederate Male Fair Confederate Male unfair Confederate

Conjunction Pain Self & Fair in Women Left Fronto-Insular Cortex 1 2 3 Fair Player Unfair Player Parameter Estimates [- 42 15 -3] Right Fronto-Insular Cortex 1 2 3 Fair Player Unfair Player Parameter Estimates [30 18 -18] Right Fronto-Insular Cortex -1 1 2 Fair Player Unfair Player Parameter Estimates [42 33 3] Left Fronto-Insular Cortex -1 1 2 Fair Player Unfair Player Parameter Estimates [- 33 33 3]

Evidence for Reward-related Activity? Pain Unfair – Pain Fair Nucleus Accumbens N.A. Gender Differences: Men – Women for Unfair - Fair 2 N.A. 1 Parameter Estimates [-9 6 -3] Women Men -1

Evidence for Correlations between Subjective Measures Of Revenge and [Pain Unfair – Pain Fair] 1 2 Women Men Subjective Ratings: Desire for Revenge Subjective Ratings -4 -2 2 4 -1 1 3 r = 0.68** N.A. Desire for Revenge Nucleus Accumbens [-9 6 -3] r = 0.08 n.s.

Conclusions Perceived fairness learned in social interactions strongly modulate empathic responses – seen in both behaviour and neural activity Loss of empathic activity seen in AI / ACC is accompanied by activity in accumbens correlates with the expressed desired for revenge to unfair individuals (in men) The data suggest gender difference which have to be pursued. This may be part of proposed proximate mechanisms behind altruistic punishment (e.g., social preference models, models of strong reciprocity; Boyd, Camerer, Gintis, Fehr, Gaechter, Rabin).

THE END Thanks to: Chris and Uta Frith Ray Dolan Geoff Bird John O'Doherty Klaas Enno Stephan Ben Seymour

Gender Difference & Intercorrelation Revenge Composite: Gender Difference & Intercorrelation Female Unfair Conspecific Male Unfair Conspecific -1 1 2 unsorry angry deserved Pain revenge * n.s. * * Rev. Angry Deser. Unsorry Rev. 1 .86** .87** .84** Angry .69** 1 .61* .62* Deserv. .95** .62* 1 .58* Unsorry .76** .14 .65** 1

An fMRI study on ‘In Vivo’ Experimental Set-up: An fMRI study on ‘In Vivo’

Trial Structure and Experimental Design Self Other Cue Stimulation 3.5 Sec. Jitter High Low 4 Sec. 2 Sec.