Contextual fear extinction ameliorates sleep disturbances found following fear conditioning in rats.

FEARFUL EXPERIENCES CAN LEAD TO ENDURING ALTERATIONS IN EMOTION AND BEHAVIOR IN HUMANS1 AND ANIMALS.2–5 FEAR CONDITIONING ASSOCIATED with these experiences is thought to be important in the development of pathophysiology underlying anxiety disorders and posttraumatic stress disorder (PTSD).9–11 Moreover, disturbances in sleep often follow a stressful or traumatic event,6 and the persistence of sleep disturbances may be predictive for future psychiatric and physical pathology.6–8 In animals, fear conditioning associated with stressful footshock training also produces marked changes in subsequent sleep.10,12,13 Specifically, the original shock training is followed by a significant decrease in subsequent REM sleep.10,14,15 Conditioned “reminders” of the shock training also decrease subsequent REM.10,14 Experimental conditioned fear involves the use of specific cues such as tone or light that presage the occurrence of footshock or less specific contextual stimuli which become associated with shock. Through pairings of cue or contextual stimuli with the occurrence of shock, these previously neutral stimuli acquire the ability to elicit a conditioned fear response (behavioral and physiological responses indicative of fear and anxiety such as behavioral freezing) when presented alone. Interestingly, though, the conditioned fear response produced by fearful cues and contexts can typically be blocked through extended presentations of either type of stimuli without the reoccurrence of footshock. This fear “extinction” is considered a type of new learning that inhibits subsequent fear without erasing the original memory for fear conditioning.16 The failure of extinction is thought to be a significant factor in persisting fear responses and anxiety.17 However, even though disturbed sleep has been associated with the continuing effects of stress, and several studies have demonstrated the effects of conditioned fear on sleep, the effects of fear extinction on subsequent sleep have yet to be examined. Therefore, the goal of this study was to determine whether fear extinction was followed by different patterns of sleep compared to those after continued fear. We trained 2 groups of rats in contextual fear using a footshock stressor and then re-exposed both groups to the fearful context alone. One group was removed from the context before extinction occurred and the other was allowed to remain in the fearful context until behavioral signs of fear (freezing) had completely subsided. Lastly, we recorded sleep in both groups after a second exposure to the fearful context without readministering footshock. This allowed us to compare the sleep of rats with extinguished fear behavior to that of rats which continued to show fear. We also examined both groups for similarities and differences in freezing during shock training and on reexposure to the context. These data demonstrate that fear extinction is associated with significantly improved sleep compared to continued fear, and may have implications for understanding the role of persisting sleep disruptions in the long-term effects of stress and trauma.