The behavioral and neural architecture of observational active avoidance is shaped by 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 a Novice, but not an Experienced, Demonstrator, suggesting that Novice and Experienced Demonstrators transmit different information to the Observer that can be used to acquire active avoidance. Shock pre-exposure enhanced avoidance in male Observers and shifted their behavioral strategy toward avoidance-preferring rather than reward-preferring responses, an effect not observed in females. 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, these activation profiles scaled with behavioral strategy: avoidance-preferring Observers showed the greatest number of correlations, balanced Observers showed fewer, and reward-preferring Observers showed the least number of correlations. Taken together, these results provide insights into the behavioral mechanisms that promote observational avoidance learning.