Freezing Displayed by Others Is a Learned Cue of Danger Resulting from Co-experiencing Own Freezing and Shock

Summary Social cues of threat are widely reported [ 1 , 2 , 3 ], whether actively produced to trigger responses in others such as alarm calls or by-products of an encounter with a predator, like the defensive behaviors themselves such as escape flights [ 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 ]. Although the recognition of social alarm cues is often innate [ 15 , 16 , 17 ], in some instances it requires experience to trigger defensive responses [ 4 , 7 ]. One mechanism proposed for how learning from self-experience contributes to social behavior is that of auto-conditioning, whereby subjects learn to associate their own behaviors with relevant trigger events. Through this process, the same behaviors, now displayed by others, gain meaning [ 18 , 19 ] (but see [ 20 ]). Although it has been shown that only animals with prior experience with shock display observational freezing [ 21 , 22 , 23 , 24 , 25 ], suggesting that auto-conditioning could mediate this process, evidence for this hypothesis was lacking. Previously we found that, when a rat freezes, the silence that results from immobility triggers observational freezing in its cage-mate, provided the cage-mate had experienced shocks before [ 24 ]. Therefore, in our study, auto-conditioning would correspond to rats learning to associate shock with their own response to it—freezing. Using a combination of behavioral and optogenetic manipulations, here, we show that freezing becomes an alarm cue by a direct association with shock. Our work shows that auto-conditioning can indeed modulate social interactions, expanding the repertoire of cues mediating social information exchange, providing a framework to study how the neural circuits involved in the self-experience of defensive behaviors overlap with the ones involved in socially triggered defensive behaviors.