Project title: Neural bases of empathic accuracy while perceiving others’ smiles

Theoretical introduction:

Most of our social interactions involve facial expressions. Understanding whether these expressions are accompanied by authentic emotional feelings is crucial in everyday life. Smile is without any doubt, the most easily recognized and yet the most nuanced among facial expressions. It can be flexibly used to communicate a wide range of emotions and critically, in many social contexts it can be voluntarily used to show that a positive emotion of amusement is felt when it is not (Ekman, 2001; Niedenthal et al., 2010). Although studies have shown that brain activity generated when making authentic vs fake expressions differs (Frank and Ekman, 1993; Coan et al., 2001; Iwase et al., 2002), the neural mechanisms underlying the ability to empathetically understanding the internal state of a target individual based on the observation of her observed smile are poorly investigated.

We hypothesized that two key brain networks, thought to support empathy, may provide such neural mechanism and would be critical for empathic accuracy (EA) when observing others’ smiles. More specifically, we hypothesized a possible role for the so called “experience sharing” (or “mirror neurons”) brain network (Zaki et al., 2012a), which include single neurons and brain areas involved in coupling the perception of social targets in a given state with the first-hand experience of the same state (di Pellegrino et al., 1992; Gallese et al., 2004; Niedenthal, 2007; Keysers et al., 2010). Additionally, we hypothesized a role for the “mentalizing” network, that is thought to include frontal midline and temporo-parietal brain areas involved in the explicit attributions of intentions and feelings to others (Saxe and Wexler, 2005; Amodio and Frith, 2006). Although recent imaging studies have suggested that both experience sharing and mentalizing networks are active during EA (Zaki et al., 2009, 2012b), to date there is no direct neuropsychological evidence showing that these networks are causally essential for EA.

Goals/Hypotheses:

The general goal of the present project is to investigate the neural bases of EA, i.e., the correspondence between the emotional feeling reported by a social target and a perceiver’s belief about that emotional feeling (Ickes and Stinson, 1990; Levenson and Ruef, 1992; Zaki et al., 2008). In particular, our aim is to test the functional relevance of experience sharing and mentalizing networks for EA when observing others making smiles. Hence, we will transiently interfere with key neural regions within these two networks to test whether they are critical for EA during perception of smiles.

Methodology:

Participants will perform an EA task in which they will be presented with naturalistic movies of actors producing smiling expressions that could be associated with positive emotional feelings (authentic amusement) or no feeling at all (no amusement, fake smiles). Participants will have to judge the authentic feeling supposedly felt by the actor and rate it in terms of emotional intensity. Performance in the EA task will be computed as the correlation between participants’ belief about the actor’s feeling and the authentic subjective feeling reported by the actor while smiling. To establish which brain region is essential for EA, we will test 5 groups of participants with no contraindication to TMS (Rossi et al., 2009). In each group, participants will perform the EA task while receiving short trains of repetitive TMS (rTMS) over a target brain region. In two counterbalanced conditions, we will administered active rTMS (to interfere with the functioning of the targeted brain region) and sham (placebo) rTMS (that will be considered the baseline condition in which no current is induced in the brain). The 5 groups will differ with respect to the specific brain region being stimulated. Experience sharing networks for observed facial expressions include brain network involved in moving and sensing the face. For this region, in two groups we will stimulate the representation of the face in the ventral premotor cortex (vPMc) and somatosensory cortex (S1). In other two groups, we will stimulate two key nodes of the mentalizing network, namely the medial prefrontal cortex (mPFC) and the temporo-parietal junction (TPJ). Lastly, in a fifth group, we will test a control region not involved in EA, namely the vertex (VTX).

Expected Results:

If experience sharing regions are critical for EA, active rTMS should impair performance relative to sham rTMS in the vPMc and S1 group. Conversely, if mentalizing regions are critical for EA, active rTMS should decrease performance in the mPFC and TPJ group. We expect no effect of active stimulation in the VTX group.

Theoretical implications and potential applications:

This project has the potential to directly test the functional relevance of experience sharing and mentalizing networks in EA and to establish which node of such networks is essential for EA. In addition to the theoretical implications for disciplines interested in empathy, this research may pave the way to more applied research.

In a clinical perspective, the exploration of the neural bases of EA may allow to implement specific psychophysiological-based assessment of patients with impaired emotion processing or poor social functioning (e.g. autism spectrum disorders, sociopathy, schizophrenia, stroke patients etc.). On the other hand, a better knowledge of the possible impaired mechanisms underlying these pathologies (e.g. embodied simulation mechanisms) may allow to develop clinical applications aimed at boosting these mechanisms with behavioral and brain stimulation methods.

References:

Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7:268–277.

Coan JA, Allen JJ, Harmon-Jones E (2001) Voluntary facial expression and hemispheric asymmetry over the frontal cortex. Psychophysiology 38:912–925.

di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp brain Res 91:176–180.

Ekman P (2001) Telling lies: Clues to deceit in the marketplace, politics, and marriage. (Norton WW, ed).

Frank M, Ekman P (1993) Not all smiles are created equal: The differences between enjoyment and nonenjoyment smiles. Humor Int J Humor … 6:9–26.

Gallese V, Keysers C, Rizzolatti G (2004) A unifying view of the basis of social cognition. Trends Cogn Sci 8:396–403.

Ickes W, Stinson L (1990) Naturalistic social cognition: Empathic accuracy in mixed-sex dyads. J Personality Soc Psychol 58:730–742.

Iwase M, Ouchi Y, Okada H, Yokoyama C, Nobezawa S, Yoshikawa E, Tsukada H, Takeda M, Yamashita K, Takeda M, Yamaguti K, Kuratsune H, Shimizu A, Watanabe Y (2002) Neural Substrates of Human Facial Expression of Pleasant Emotion Induced by Comic Films: A PET Study. Neuroimage 17:758–768.

Keysers C, Kaas JH, Gazzola V (2010) Somatosensation in social perception. Nat Rev Neurosci 11:417–428.

Levenson RW, Ruef AM (1992) Empathy: a physiological substrate. J Pers Soc Psychol 63:234–246.

Niedenthal PM (2007) Embodying emotion. Science 316:1002–1005.

Niedenthal PM, Mermillod M, Maringer M, Hess U (2010) The Simulation of Smiles (SIMS) model: Embodied simulation and the meaning of facial expression. Behav Brain Sci 33:417–433; discussion 433–480.

Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039.

Saxe R, Wexler A (2005) Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia 43:1391–1399.

Zaki J, Bolger N, Ochsner K (2008) It Takes Two The Interpersonal Nature of Empathic Accuracy. Psychol Sci 19:399–404.

Zaki J, Ochsner KN, Ochsner K (2012a) The neuroscience of empathy: progress, pitfalls and promise. Nat Neurosci 15:675–680.

Zaki J, Weber J, Bolger N, Ochsner K (2009) The neural bases of empathic accuracy. Proc Natl Acad Sci U S A 106:11382–11387.

Zaki J, Weber J, Ochsner K (2012b) Task-dependent neural bases of perceiving emotionally expressive targets. Front Hum Neurosci 6:228.

Attività formativa dell’assegnista:

L’attività formativa sarà incentrata su:

1 - approfondimento delle conoscenze dei modelli teorici fondamentali e delle principali aree tematiche riguardanti le neuroscienze cognitive, in generale, e della percezione sociale, riconoscimento di emozioni e dell’empatia, in particolare.

2 - acquisizione della metodologia di ricerca scientifica (qualitativa e quantitativa) per la progettazione e la realizzazione di progetti di ricerca nelle neuroscienze cognitive;

3 - acquisizione delle conoscenze sulle tecniche di analisi statistiche appropriate con l’utilizzo dei più significativi pacchetti statistici;

4 - acquisizione delle competenze tecniche e teoriche per l’utilizzo della stimolazione magnetica transcranica (TMS);

5 - acquisizione di competenze di ideazione, progettazione, realizzazione di un progetto di ricerca scientifica;

6 - acquisizione delle competenze per la diffusione dei risultati della ricerca scientifica (congressi nazionali ed internazionali e pubblicazioni scientifiche nazionali e internazionali);

7 - acquisizione delle competenze per l’applicazione dei risultati della ricerca scientifica per l’ideazione e lo sviluppo di nuovi trattamenti riabilitativi.

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