Social Perspective-taking Shapes Brain Hemodynamic Activity and Eye Movements During Movie Viewing

Mareike Bacha-Trams; Elisa Ryyppö; Enrico Glerean; Mikko Sams; Iiro P. Jääskeläinen

Disclosures

Soc Cogn Affect Neurosci. 2020;15(2):175-191. 

In This Article

Abstract and Introduction

Abstract

Putting oneself into the shoes of others is an important aspect of social cognition. We measured brain hemodynamic activity and eye-gaze patterns while participants were viewing a shortened version of the movie 'My Sister's Keeper' from two perspectives: that of a potential organ donor, who violates moral norms by refusing to donate her kidney, and that of a potential organ recipient, who suffers in pain. Inter-subject correlation (ISC) of brain activity was significantly higher during the potential organ donor's perspective in dorsolateral and inferior prefrontal, lateral and inferior occipital, and inferior–anterior temporal areas. In the reverse contrast, stronger ISC was observed in superior temporal, posterior frontal and anterior parietal areas. Eye-gaze analysis showed higher proportion of fixations on the potential organ recipient during both perspectives. Taken together, these results suggest that during social perspective-taking different brain areas can be flexibly recruited depending on the nature of the perspective that is taken.

Introduction

Perspective-taking is an important aspect of human social cognition. To perceive and understand the world around us in a similar way is necessary for reaching a common ground and smooth communication. This involves both the physical environment and social situations between people. One possibility to achieve shared understanding of a situation is to adopt the same psychological perspective. By the process of social perspective-taking, the own point of view is temporarily suspended in order to simulate and view a situation from another person's different angle (Epley and Caruso, 2008).

Social perspective-taking requires building of an internal model or schema to be able to interpret the unfolding events, actions and interactions with task-relevant objects from the perspective of the other person. Social perspective-taking is a relevant factor in society as several studies indicate that it has a positive impact on social interactions and relations: perspective-taking can alleviate bias between groups (Todd et al., 2012) and increases individuals' willingness to interact with out-group participants (Wang et al., 2014), thus facilitating in-group/out-group exchanges (Galinsky and Moskowitz, 2000). Perspective-taking could also provide an advantage in different types of negotiations (Galinsky et al., 2008). Further, perspective-taking could provide one important underlying mechanism for empathy, as one needs to put oneself in the position of someone else in order to feel the way he/she feels (Leong et al., 2015).

Behavioural studies with participants sharing the same psychological perspective have shown that the interpretation of simple visual scenes (Kaakinen et al., 2011) and the recall of expository text (Kaakinen et al., 2002; Kaakinen et al., 2003) are similar across individuals. Furthermore, it has been shown that both brain responses to specific objects in dynamic visual scenes and the related semantic categories are shaped by directing the participants' attention towards them (Çukur et al., 2013). Similarly, attention may be directed to task-relevant sensory information when sharing a psychological perspective.

Furthermore, a distinction between cognitive and affective perspective-taking has been made before: while cognitive perspective-taking implies the ability to understand thoughts and beliefs of another individual, affective perspective-taking is focused on inferring another person's emotions and feelings. Brain imaging studies with functional magnetic resonance imaging (fMRI), using cartoons or written scenarios, have shown that the neural correlates of cognitive and affective perspective-taking are partly shared for both and involve brain areas as, e.g. temporoparietal junction and precuneus. Yet they also are dissociable from one another, with, e.g. cingulate cortex and limbic and basal ganglia structures uniquely involved in affective perspective-taking (Völlm et al., 2006; Bodden et al., 2013; Schlaffke et al., 2015). In addition, differences were found within the frontal lobes between cognitive and affective perspective-taking: while cognitive perspective-taking elicited additional activation in the middle frontal gyrus, lateral orbitofrontal cortex, superior temporal gyrus and ventromedial prefrontal cortex (vmPFC), the medial orbitofrontal cortex was more strongly involved in affective perspective-taking (Hynes et al., 2006; Sebastian et al., 2012; Corradi-Dell'Acqua et al. 2014). Complementary findings of Kalbe et al. (2010), using transcranial magnetic stimulation applied to the right dorsolateral prefrontal cortex (DLPFC) to reduce cortical excitability when healthy male subjects performed a perspective-taking task, showed selective impairment of cognitive but not affective perspective-taking during the stimulation.

Developments in functional magnetic resonance imaging (fMRI) data analysis algorithms (Bartels and Zeki, 2004; Hasson et al., 2004) have enabled investigation of socially complex interactions and their underlying neural correlates using movies as ecologically valid stimuli. Social stimuli tend to have ambiguous and convergent features that may be overlooked in isolated test settings. To overcome these limitations, many recent studies have successfully used rich stimulus environments to investigate perceptual brain functions with the aim of approaching the complexity of real life (e.g. Bartels and Zeki, 2004; Malinen et al., 2007; Ylipaavalniemi et al., 2009; Lahnakoski et al., 2012). Greater sensitivity has also been shown in the clinical assessment of neuropsychiatric populations: impairment, e.g. in inferring an emotion from a static display of a facial expression, does not automatically have to translate into difficulty in interring emotions in real life, as the respective emotion in real life will co-occur with other behavioural cues (Fernandez-Duque et al., 2010). These studies not only show the feasibility of such complex ecologically valid approaches (although recognising the obvious challenges in signal analysis due to the complexity of the recorded signals), but further indicate that using ecologically valid stimuli (in contrast to more standardised and less complex approaches) is particularly important in studies comprising multidimensional social interactions in order to make them as credible and perceptible as possible.

Thus, in this study, a movie was used as an ecologically valid stimulus during fMRI. The data were analysed using inter-subject correlation (ISC) of brain hemodynamic activity, which provides a model-free analysis approach and does not require any a priori model of the stimulus giving rise to the fMRI signal. In ISC the brains of individual subjects are aligned, and the correlations between the hemodynamic activity time courses for each voxel are calculated across all subject pairs, in order to examine the degree of similarity in individual brains' responses to the common movie stimulus. ISC can thus be interpreted as reflecting synchronised neural activity or similarity of cerebral information processing across individuals (Hasson et al., 2004; Malinen et al. 2006; Wilson et al., 2008; Kauppi et al., 2010), solely based on similarities between the subjects' brain responses when they react to the various aspects of the complex stimulus (Hasson et al., 2010). It has been shown with fMRI that during movie watching, not only basic sensory cortices but also 'higher-order' prefrontal cortical areas exhibit ISC of brain activity across participants (Jääskeläinen et al., 2008; Hasson et al., 2008). In addition, reliability and sensitivity of ISC to detect involved brain areas in complex experimental setups have been shown to be at the same level as in model-based analyses (Pajula et al., 2012).

Similarities in how the brains of individual participants process the events in the movie, measured as ISC, may provide an important mechanism for similar information processing across study participants and form the basis of shared psychological perspective-taking. Therefore, ISC is particularly suited to examine social perspective-taking induced by movies. However, note that without any specific instructions on how to take perspective when viewing a movie, of course, the participants' similar viewing experience is based on how the movie director leads the viewer using techniques of cinematographic art (Hasson et al., 2010).

One previous study investigating perspective-taking effects on brain activity used movie clips that the participants watched during fMRI (Lahnakoski et al., 2014). Perspective-taking was observed to modulate brain activity in higher-order visual areas and inferior occipitotemporal areas. In this previous study, however, the participants adopted either a social perspective (forensic detective) or non-social perspective (interior decorator). It has not yet been addressed how taking two contrasting social perspectives, i.e. the perspective of one vs other movie protagonist in a drama movie, modulates information processing in the brain.

The present results were collected as a part of a larger dataset. We studied 30 participants watching a 24-min movie segment (modified from 'My sister's keeper' dir. Nick Cassavetes, 2009, Curmudgeon Films) during fMRI. The movie depicts a moral dilemma between two sisters. The protagonist Anna (potential organ donor) refuses to donate one of her kidneys to her sister Kate who is fatally ill from cancer (potential organ recipient). Due to Anna's refusal, Kate dies. In two previously published studies, two aspects of this dataset were analysed. In the first, the participants' brain activity patterns were compared when the participants assumed that the sisters were either genetic sisters or that the younger sister Anna had been adopted as a newborn (Bacha-Trams et al., 2017). Analysing the ISC between participants in the two different conditions, this study showed significantly stronger correlations of brain activity patterns when the subjects believed that the sisters were genetically related particularly in the insula, cingulate, medial and lateral prefrontal, superior temporal and superior parietal cortices, thus areas which have been previously associated with processes such as moral and emotional conflict regulation, decision-making and mentalising. Although 90% of the subjects self-reported that genetic relationship was not relevant for the viewing experience, these results suggest that the mere knowledge of a genetic relationship between interacting persons modulated robustly the brain activity during film viewing.

In the second published study, we investigated how subjects with holistic and analytical thinking styles, as determined based on self-report questionnaire scores, differentially perceived the movie (Bacha-Trams et al., 2018). In general, holistic thinkers are known to view background and objects more as a whole, by taking context into account, whereas analytical thinkers focus more on details such as perceptual objects at the expense of context. Holistic thinkers showed significant ISC in more extensive cortical areas than analytical thinkers, particularly in occipital, prefrontal and temporal cortices, suggesting that they perceived the movie in a more similar fashion, while in analytical thinkers, significant ISC was observed in right hemisphere fusiform gyrus, temporoparietal junction and frontal cortex.

In the present study, we analysed how adopting a social perspective of one or the other of the movie protagonists was reflected in the brain activity of the participants. These novel results were neither analysed nor reported in the two previously published studies.

Further, eye-gaze patterns and physiological responses (heart rate and breathing rate) were recorded during fMRI as the participants were viewing the movie. We hypothesised that there would be differences in eye-gaze patterns as well as in brain regions recruited, as indicated by differences in ISC, during the two perspectives. More specifically, as the two perspectives differ in their cognitive load, we hypothesised to find activations in brain areas associated with processing of moral dilemma, conflict monitoring and self-reflection during the perspective of the potential organ donor undergoing the moral dilemma (to donate an organ or not) and differentiable brain activity associated with empathy for the perspective of the sister suffering from terminal cancer. We further hypothesised that the subjects would prefer to watch the character whose perspective they were taking is disclosed by eye tracking.

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