Behavioral and neural architecture of observational active avoidance: Effects of demonstrator experience and observer sex

Observational learning allows an individual to gain information about potential outcomes and is particularly advantageous when learning to actively avoid danger without risking harm to oneself. To assess observational learning of active avoidance, Observer rats witnessed Demonstrator rats undergo platform-mediated avoidance (PMA), in which rats learn to avoid a tone-signaled footshock by stepping onto a safe platform. We found that Observers’ avoidance was correlated with that of a Novice, but not of an Experienced, Demonstrator, suggesting that Novice and Experienced Demonstrators transmit different information to the Observer that is used to acquire active avoidance. Additionally, PMA acquisition improved in males when Observers were given a footshock prior to observational learning. Shock pre-exposure also altered the behavioral strategy used by male, but not female, Observers such that shock pre-exposed males adopted avoidance-preferring over reward-preferring strategies. We then used c-Fos immunohistochemistry to quantify neural activation in brain areas previously implicated in direct learning of active avoidance. Observers that witnessed Experienced Demonstrators showed more correlations in activation between brain areas than Observers that witnessed a Novice Demonstrator. Furthermore, avoidance-preferring Observers showed more correlations in activation than reward-preferring Observers. Taken together, these results provide insights into the behavioral mechanisms that promote observational avoidance learning and identify potential neural targets for research investigating social learning deficits in neuropsychiatric disease.