A Brain-To-Brain Mechanism for Social Transmission of Threat Learning.

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.