Cingulate dependent social risk assessment in rats

Abstract

Social transmission of distress has been conceived of as a one-way phenomenon in which an observer catches the emotions of another. Here we use a paradigm in which an observer rat witnesses another receive electroshocks. Bayesian model comparison and Granger causality argue against this one-way vision in favor of bidirectional information transfer: how the observer reacts to the demonstrator's distress influences the behavior of the demonstrator. Intriguingly, this was true to a similar extent across highly familiar and entirely unfamiliar rats. Injecting muscimol in the anterior cingulate of observers reduced freezing in the observers and in the demonstrators receiving the shocks. That rats share the distress of unfamiliar strains is at odds with evolutionary thinking that empathy should be biased towards close individuals. Using simulations, we support the complementary notion that distress transmission could be selected to more efficiently detect dangers in a group.

Emotional Mirror Neurons in the Rat’s Anterior Cingulate Cortex

“…Third, our animals showed unusually low freezing during the electrophysiological ShockObs condition compared to previous behavioral experiments and the present muscimol study [ 14 , 15 , 35 ]. Traditionally, we tested animals in the week following pre-exposure, in a two-compartment cage resembling that during pre-exposure and without tethering [ 14 , 15 , 35 ]. For electrophysiology, we introduced 2 additional weeks of habituation, placed the observer on a plastic cylinder to avoid electrical noise, and tethered the animal.…”

“…p values refer to uncorrected, two-sample two-tailed t tests across the two groups. Note that the data from the ShockObs but not the CS condition are also used to explore how this affects the behavior of the demonstrator in [ 35 ]. …”

“…Such changes in context are known to reduce freezing in fear conditioning [ 39 ], and we believe this to have reduced the propensity to freeze. That the ACC nevertheless encoded ShockObs vigorously is notable, but experiments that quantify ACC responses as a function of the remoteness (in time and contextual similarity) of pre-exposure will shed light onto what the ACC represents: if ACC responses decrease with increasing safety cues, they are more likely to represent the observer’s personal risk assessment [ 35 ]. If responses remain constant, they are more likely to represent the distress of the other.…”

“…Finally, there is an important distinction between emotional contagion and empathy. Recruiting neurons involved in one’s own experience of pain while witnessing the pain of others could suffice to trigger emotional contagion—feeling the distress that the observed animal feels—and can prepare the observer to face the danger that afflicted the demonstrator [ 35 ]. This, however, does not provide evidence that the observer understands that this vicarious pain is experienced by a specific other animal—as empathy proper would require.…”

Harm to others acts as a cingulate dependent negative reinforcer in rat

“…The Bayes factor for including a familiarity*session was BF10 = .80, which is inconclusive. Accordingly, familiarity is not necessary for reducing lever preference, in line with data showing that rats freeze even when an unfamiliar conspecific gets a shock [19] and free an unfamiliar trapped rat [20]. However we cannot exclude that familiarity may have a subtle effect on the magnitude of switching, as shown in mice [21][22][23][24][25].…”