A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning

Yafeng Pan*, Mikkel C. Vinding, Lei Zhang, Daniel Lundqvist, Andreas Olsson*

*Corresponding author for this work

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Abstract

Survival and adaptation in environments require swift and efficacious learning about what is dangerous. Across species, much of such threat learning is acquired socially, e.g., through the observation of others’ (“demonstrators’”) defensive behaviors. However, the specific neural mechanisms responsible for the integration of information shared between demonstrators and observers remain largely unknown. This dearth of knowledge is addressed by performing magnetoencephalography (MEG) neuroimaging in demonstrator‐observer dyads. A set of stimuli are first shown to a demonstrator whose defensive responses are filmed and later presented to an observer, while neuronal activity is recorded sequentially from both individuals who never interacted directly. These results show that brain‐to‐brain coupling (BtBC) in the fronto‐limbic circuit (including insula, ventromedial, and dorsolateral prefrontal cortex) within demonstrator‐observer dyads predict subsequent expressions of learning in the observer. Importantly, the predictive power of BtBC magnifies when a threat is imminent to the demonstrator. Furthermore, BtBC depends on how observers perceive their social status relative to the demonstrator, likely driven by shared attention and emotion, as bolstered by dyadic pupillary coupling. Taken together, this study describes a brain‐to‐brain mechanism for social threat learning, involving BtBC, which reflects social relationships and predicts adaptive, learned behaviors.
Original languageEnglish
Article number2304037
JournalAdvanced Science
Early online date6 Aug 2023
DOIs
Publication statusE-pub ahead of print - 6 Aug 2023

Bibliographical note

Acknowledgements:
The authors would like to thank Tabea Eimer, Colin Jones, Claire Pleche, Andreas Henriksson, Anton Toftgård, and Daniel Sortebech for their assistance in data collection. The authors thank the two anonymous reviewers for their insightful comments and suggestions. Funding is provided by the Knut and Alice Wallenberg Foundation (KAW 2014.0237) and a Consolidator Grant (2018-00877) from the Swedish Research Council (VR) to A.O, the National Natural Science Foundation of China (No. 62 207 025), the Humanities and Social Sciences Research Project from the Ministry of Education of China (No. 22YJC190017), and the Fundamental Research Funds for the Central Universities to Y.P. MEG data for this study are collected at NatMEG, the National Facility for Magnetoencephalography (www.natmeg.se), Karolinska Institutet, Sweden. The NatMEG facility is supported by the Knut and Alice Wallenberg Foundation (KAW 2011.0207). MRI data collection is supported by a grant to the Stockholm University Brain Imaging Centre (SU FV-5.1.2-1035-15). Structural MRI from three observers is retrieved from the IronAge study database, which is financially supported by the Swedish Research Council.

Keywords

  • vicarious fear
  • social status
  • brain‐to‐brain coupling (BtBC)
  • observational threat learning
  • Magnetoencephalography (MEG)

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