Abstract
Social transmission of freezing behavior has been conceived of as a one-way phenomenon in which an observer “catches” the fear of another. Here, we use a paradigm in which an observer rat witnesses another rat receiving electroshocks. Bayesian model comparison and Granger causality show that rats exchange information about danger in both directions: how the observer reacts to the demonstrator’s distress also influences how the demonstrator responds to the danger. This was true to a similar extent across highly familiar and entirely unfamiliar rats but is stronger in animals preexposed to shocks. Injecting muscimol in the anterior cingulate of observers reduced freezing in the observers and in the demonstrators receiving the shocks. Using simulations, we support the notion that the coupling of freezing across rats could be selected for to more efficiently detect dangers in a group, in a way similar to cross-species eavesdropping.
Highlights
The ability to anticipate threats and deploy defensive responses appropriately is key to survival [1]
Following extensive evidence that humans witnessing the pain of others show (1) brain activity as if they had been in pain themselves [2,3,4,5] and (2) defensive changes in cortical excitability reminiscent of the freezing behavior found in animals [6,7], two separate streams of research have shown that rodents are sensitive to the emotional state of others (Fig 1)
In the second experiment, all demonstrator–observer dyads were unfamiliar with the animal they were paired with during the interaction test but differed in whether rats were familiar with the strain of their pair-mate or were unfamiliar with that strain
Summary
The ability to anticipate threats and deploy defensive responses appropriately is key to survival [1]. Rodents freeze less to a fear-conditioned stimulus when they are paired with a conspecific that does not engage in freezing [15,16,17,18,19,20,21,22,23,24,25]. These observations suggest that rodents have evolved mechanisms to more selectively deploy defensive behavior in anticipation of a danger by using the response of conspecifics as evidence for or against the presence of the danger.
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