Causal manipulation of self-other mergence in the dorsomedial prefrontal cortex

Marco K Wittmann,Nadescha Trudel,Hailey A Trier,Miriam C Klein-Flügge,Alejandra Sel,Lennart Verhagen,Matthew F.S Rushworth

doi:10.1016/j.neuron.2021.05.027

Abstract

SummaryTo navigate social environments, people must simultaneously hold representations about their own and others’ abilities. During self-other mergence, people estimate others’ abilities not only on the basis of the others’ past performance, but the estimates are also influenced by their own performance. For example, if we perform well, we overestimate the abilities of those with whom we are co-operating and underestimate competitors. Self-other mergence is associated with specific activity patterns in the dorsomedial prefrontal cortex (dmPFC). Using a combination of non-invasive brain stimulation, functional magnetic resonance imaging, and computational modeling, we show that dmPFC neurostimulation silences these neural signatures of self-other mergence in relation to estimation of others’ abilities. In consequence, self-other mergence behavior increases, and our assessments of our own performance are projected increasingly onto other people. This suggests an inherent tendency to form interdependent social representations and a causal role of the dmPFC in separating self and other representations.

Highlights

Navigating social environments requires us to interact with other agents that behave to ourselves
self-other mergence (SOM) has been linked to activity in the medial prefrontal cortex
The strength of SOM effects correlates with functional magnetic resonance imaging (fMRI) signal strength in Neurostimulation protocol Here we used the same experimental paradigm to causally manipulate SOM by targeting its neural correlates in the dorsomedial prefrontal cortex (dmPFC) with 40-s continuous theta burst stimulation (Huang et al, 2005; Polanıa et al, 2018) while recording the effect of this causal intervention on behavioral measurements of SOM and simultaneously acquired neural measurements of SOM. cTBS is an offline brain stimulation protocol that decreases cortical excitability of the targeted region for several minutes after application (Huang et al, 2005). cTBS has been used to modulate cortical excitability in motor areas and in brain areas relevant for social cognition (Hill et al, 2017) and metacognition (Miyamoto et al, 2021)

Summary

Introduction

Navigating social environments requires us to interact with other agents that behave to ourselves. Other people’s decisions influence how we decide ourselves (Garvert et al, 2015; Suzuki et al, 2016), and we keep estimates of our own and other people’s performance levels and abilities (Boorman et al, 2013; Wittmann et al, 2016). Ability estimates—impressions of how well we and others perform certain actions—allow us to construct shared representations of ourselves and others when we pursue cooperative goals or compete against each other. Representations of ourselves change dynamically with social context (Wittmann et al, 2018). We investigate the causal contribution of the dorsomedial prefrontal cortex (dmPFC) to maintaining an individualized sense of one’s own and others’ abilities. We show that estimates of our own abilities are merged increasingly with estimates of others’ abilities after causal manipulation of the medial prefrontal cortex

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