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

• Published in: Current biology Vol. 30; no. 6; pp. 1128 - 1135.e6
• Main Authors: Cruz, Andreia, Heinemans, Mirjam, Márquez, Cristina, Moita, Marta A.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 23.03.2020
• Subjects: 2MT; auto-conditioning; fear; looming stimulus; rodents; social behavior; vlPAG; vlPAG; auto-conditioning; looming stimulus; social behavior; 2MT; rodents; fear
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2020.01.025

Social cues of threat are widely reported [1–3], 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 [4–14]. Although the recognition of social alarm cues is often innate [15–17], 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 [21–25], 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. •Stress-induced sensitization by itself does not promote observational freezing•Aversive shocks promote observational freezing if rats freeze during shock exposure•Observational freezing is not enabled by self-experience with freezing without shock•Optogenetically induced freezing paired with shock enables observational freezing Through auto-conditioning, subjects learn to associate their own behaviors with relevant trigger events. Thereby, the same behaviors, now displayed by others, gain meaning. Cruz et al. show that auto-conditioning, in particular the acquisition of freezing-shock association, mediates the ability of rats to use freezing by others as an alarm cue.