Conditioned turning behavior: a Pavlovian fear response expressed during the post-encounter period following aversive stimulation

Rats were trained to fear an auditory conditioned stimulus (CS) by pairing it with a mild electric shock (the unconditioned stimulus, or US) delivered to one eyelid. After training, the CS elicited two different conditioned fear responses from rats: a passive freezing response, and an active turning response. The balance between these two modes of conditioned responding depended upon the rat's recent history of encounters with the US. If rats had not recently encountered the US, then they responded to the CS by freezing. But after recently encountering the US, rats exhibited CS-evoked turning responses that were always directed away from the trained eyelid, even if the US had recently been delivered to the opposite (untrained) eyelid. This post-encounter turning behavior was not observed in rats that had been trained with unpaired presentations of the CS and US, indicating that even though CS-evoked turning was selectively expressed after recent encounters with the US, it was nonetheless a conditioned Pavlovian fear response that depended upon a learned association between the CS and US. Further supporting this conclusion, pharmacological inactivation experiments showed that expression of both freezing and turning behaviors depended upon lateralized circuits in the amygdala and periaqueductal gray (PAG) that are known to support expression of Pavlovian fear responses. These findings indicate that even though the ability of a CS to elicit Pavlovian fear responses depend upon the long-term history of CS-US pairings, the mode of conditioned responding (freezing versus turning in the present experiments) can be modulated by short-term factors, such as the recent history of US encounters. We discuss neural mechanisms that might mediate such short-term transitions between different modes of defensive responding, and consider how dysregulation of such mechanisms might contribute to clinical anxiety disorders.