Freezing displayed by others is a learned cue of danger resulting from co-experiencing own-freezing and shock

Abstract

SUMMARYSocial cues of threat are widely reported [1–3], whether actively produced to trigger responses in others, such as the emission of alarm calls, or by-products of an encounter with a predator, like the defensive behaviors themselves, such as an escape flight [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 the 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]. Hence, 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 that mediate 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.

Harm to Others Acts as a Negative Reinforcer in Rats

“…Sample size (N) reflects the number of actors included in the behavioral analyses. switching, in line with prior studies showing that prior experience increases sensitivity to others' pain as measured by vicarious freezing [9,16,19,21,22]. The behavior of the victim, in terms of USVs, pain squeaks, and freezing, in contrast, was not robustly associated with switching, but victims that decreased their time spent close to the divider (due to shockinduced behavioral activity) were paired with actors with higher switching scores.…”

“…Third, we show that pre-exposure to shocks potentiates switching. It has been shown that freezing while observing another animal receive shocks is potentiated by prior shock experience [9,19,21,47], but other arousing experiences, such as a forced swim test, do not have the same potentiating effect [22,48]. Moreover, although [32,35] for muscimol (red) and saline (green) animals.…”

“…Prior experience with footshocks increases the sensitivity of rodents to witnessing footshocks in others [9,16,19,21,22]. Does prior experience also influence switching in our paradigm?…”

Distinct circuits in rat central amygdala for defensive behaviors evoked by socially signaled imminent versus remote danger

“…15,16 It was proposed that during such pre-exposure, observers learn to associate freezing with aversive sensory stimulation, which makes emotional contagion possible. 40 Our data show that social information can elicit robust and flexible behavioral responses without any prior training, possibly through engaging different mechanisms-that is, change of the observers' state.…”

Pro-social preference in an automated operant two-choice reward task under different housing conditions: Exploratory studies on pro-social decision making

“…A number of studies have examined vicarious freezing behavior as an indicator of empathy in rodents ( Atsak et al, 2011 ; Carrillo et al, 2019 ; Cruz et al, 2020 ; Han et al, 2020 ; Jeon et al, 2010 ; Pereira et al, 2012 ). In these studies usually an observer witnesses a demonstrator experience some kind of threat, most often a foot shock.…”