Influence of cognitive stance and physical perspective on subjective and autonomic reactivity to observed pain and pleasure: An immersive virtual reality study

Highlights

• Virtual Pain and Pleasure elicit reactivity similar to that induced by real stimuli.

• Physical perspective is fundamental for inducing ownership on the virtual hand.

• Pain stimuli bring about maximal SCRs regardless of the physical perspective.

• Physiological reactivity is reduced when taking Other-Oriented stance.

• Other-Oriented stance induces highest affective and intensity ratings.

Abstract

Observing others’ pain may induce a reaction called personal distress that may be influenced by top-down (imagine self or other in pain, i.e., self- vs other-oriented stance) and bottom-up (physical perspective of those who suffer, i.e., first vs third person perspective- 1PP vs 3PP) processes. The different contributions of these processes have not been teased apart. By capitalizing on the power of Immersive Virtual Reality, we explored how behavioural (subjective ratings) and physiological reactivity (skin conductance reactivity, SCR) to pain and pleasure delivered to an avatar was influenced by Cognitive stance and Physical perspective. Taking an Other-Oriented stance leads to attributing higher congruent valence (i.e. pain rated as unpleasant and pleasure as pleasant) and intensity to the stimuli and induces reduced SCR. Ownership over the virtual limb was maximal in 1PP where physiological reactivity to the stimuli was comparable. Our results highlight different components underpinning reactivity to pain and pleasure.

Introduction

The inter-individual sharing of emotions, feelings and beliefs characterize human social interactions, a condition that is constitutive of empathy. This multidimensional construct includes a variety of components ranging from the automatic and involuntary reactivity that occurs on the self when we see others (e.g. sensorimotor contagion) to the other-oriented stance that allows us to understand others through cognition (e.g. perspective-taking) (Davis, 1980, Decety and Jackson, 2004). Studies on empathy for pain indicate that people who see or imagine others in pain tend to empathically share what others feel at both behavioral and neural levels (Betti and Aglioti, 2016, Lamm et al., 2011). Contrary to empathic concern (which maintains a clear self-other distinction), sensorimotor contagion is likely to (1) increase the personal distress in the observer (e.g. when witnessing painful stimuli being delivered to others) (Batson et al., 1997) and (2) lead to ego-centered reactivity. In contrast, perspective-taking, i.e. the mechanism that allows one to project self upon another individual (Davis, 1980), may allow one to take a distinct stance and consequently react with an adequate response. Taking the perspective of another may occur at two main levels, namely at the perceptual (i.e. seeing the state of a model in first vs. third person perspective) and the cognitive (i.e. imagining feeling the same state observed or imagined in others or imagining the feelings of others in a given state) level (Chiu and Yeh, 2017). More specifically, visual perspective-taking reflects the physical point-of-view (e.g., seeing painful stimuli in different perspectives), while the cognitive perspective-taking refers to a specific attributional stance (e.g. reports of what seen in others would feel like on them or on the self).

Neuroimaging and neurophysiological studies have investigated the contribution of visual and cognitive perspective-taking in the observation of pain in others (Abu-Akel et al., 2014, Avenanti et al., 2006, Bucchioni et al., 2016; Drwecki et al., 2011; Jackson, Brunet, Meltzoff, & Decety, 2006; Lamm et al., 2007a, Lamm et al., 2007b, 2008; Leong et al., 2015; Vistoli, Achim, Lavoie, & Jackson, 2016). For instance, Jackson et al. (2006) explored cognitive perspective-taking by asking participants to observe pictures of others in pain and to imagine and rate the level of the perceived pain from different perspectives (self or other). Results showed that adopting the other’s perspective induced a specific increase in the right temporo-parietal junction, renowned for playing a crucial role in perspective-taking. Bucchioni et al. (2016) found that observing images of hands receiving painful stimulation, inhibits the motor cortex activity only if the hands appear in first-person perspective (1PP) - not when rotated 180° (third-person perspective, 3PP). Recently, Vistoli et al. (2016) manipulated both the visual perspective (1PP and 3PP) and the cognitive stance (imagine oneself or another person in the painful or neutral situation) and showed that the visual perspective-taking modulates the activity of the temporo-parietal junction during the observation of pain (Lamm et al., 2011) which consequently became more activated when observing others in pain in 1PP than in 3PP. This result suggests that the cognitive perspective-taking can be influenced in a bottom-up way for example by changes in the visual perspective.

Advances in computer graphics over the last two decades allowed researchers to use Immersive Virtual Reality (IVR) as a new and powerful tool for psychology and neuroscience (Bohil et al., 2011, Monti and Aglioti, 2018, Pan and Hamilton, 2018, Sanchez-Vives and Slater, 2005, Tieri et al., 2018). Expanding on classical studies that investigated the induction of illusory Feelings of Ownership (FO), i.e. the illusion that an external hand belong to own body (e.g., the rubber hand illusion, Botvinick & Cohen, 1998), IVR studies show that FO over a virtual body part can be easily induced by presenting a virtual body in 1PP; by means of a Head Mounted Display (HMD) (Maselli and Slater, 2013, Maselli and Slater, 2014, Petkova and Ehrsson, 2008, Petkova et al., 2011, Slater et al., 2010). In the same vein, we recently observed that the mere passive observation of a virtual limb from a 1PP (without any multisensory visuo-tactile or visuo-motor boosting) is sufficient to elicit FO at explicit (e.g., questionnaire answers; Tieri, Tidoni, Pavone, & Aglioti, 2015a) and implicit [e.g. skin conductance response (SCR; Fusaro et al., 2016, Tieri et al., 2015b), thermoregulation (Tieri, Gioia, Scandola, Pavone, & Aglioti, 2017) and electroencephalographic response (Pavone et al., 2016; Pezzetta et al., 2018; Spinelli, Tieri, Pavone, & Aglioti, 2018) levels.

It is worth noting that while IVR has been used for exploring empathy for pain (Bouchard et al., 2013, Fusaro et al., 2016, Jackson et al., 2015) the study of empathy for positive states (e.g. the conditions in which imagining, recalling and observing joy in others triggers a positive state of mind in the empathizer) is still in its infancy (Paracampo, Pirruccio, Costa, Borgomaneri, & Avenanti, 2018). Importantly, however, pleasant touch represents an important element in interpersonal connections and leads to positive feelings that forge attachment and social bonds (Suvilehto, Glerean, Dunbar, Hari, & Nummenmaa, 2015). Yet, while studies started to focus on the (cognitive and visual) perspective-taking responses to painful stimulation (Bucchioni et al., 2016, Jackson et al., 2006, Vistoli et al., 2016) less attention has been paid to whether pleasant touch is also influenced by manipulating physical perspective and cognitive stance. By using IVR presented through an HMD, we explored how taking a different physical perspective (1PP vs 3PP) modulates the behavioral and the physiological (Skin Conductance Responses- SCR and Heart Rate) reactivity in participants who observe virtual painful and pleasant stimuli delivered on (i) a virtual body that was embodied when seen from 1PP or (ii) on another avatar seated in the opposite side of a table (3PP). Results showed that both behavioral and physiological effects were qualitatively comparable in the two physical perspectives (Fusaro et al., 2016).

In the present study, building upon previous research, we used IVR to investigate (i) how the physical perspective (i.e., avatar seen from 1PP vs. 3PP) could influence the subjective (Visuo Analogue Scale, VAS) and physiological (SCRs) responses to the observation of virtual stimuli (representing pain and pleasure) on self and others and, importantly, (ii) whether these responses are modulated by the top-down information related to the cognitive stance (reports while in Self- vs. Other- shoes) and how.