Four experiments used rats to study false context fear memories. In Experiment 1, rats were pre-exposed to a distinctive chamber (context A) or to a control environment (context C), shocked after a delay in a second chamber (context B) and tested either in B or A. Rats pre-exposed to A froze just as much as control rats in B but more than control rats in A. In Experiment 2, rats were pre-exposed to A or C, subjected to an immediate shock in B and tested in B or A. Rats pre-exposed to A froze when tested in A but did not freeze when tested in B and control rats did not freeze in either A or B. The false fear memory to the pre-exposed A was contingent on its similarity with the shocked B. In Experiment 3, rats pre-exposed to A and subjected to immediate shock in B froze when tested in A but did not freeze when tested in C and rats pre-exposed to C did not freeze when tested either in A or C. In Experiment 4, rats pre-exposed to A and subjected to immediate shock in B froze more when tested in A than rats whose pre-exposure to A began with an immediate shock. The results were discussed in terms of a dual systems explanation of context fear conditioning: a hippocampal-dependent process that forms a unitary representation of context and an amygdala-based process which associates this representation with shock.Rats learn to fear a context (a distinctive chamber) in which they receive brief but aversive footshock. This learning is thought to involve two distinct systems. The first, hippocampal-dependent system records the conjunctions among the array of cues (the surfaces, texture of the floor, shape, and so on) and combines this information into a unitized representation of the context (e.g., McLaren et al. 1989;Sutherland and Rudy 1989;Fanselow 1990;O'Reilly and Rudy 2001). The second, amygdala-dependent system forms excitatory associations between this unitized representation of the context and the fear motivational system elicited by the aversive shock unconditioned stimulus (US). The consequence of these associations is that rats exhibit fear responses when re-exposed to that now conditioned context (e.g., Davis 1990). The interaction of these two systems explains the relation between the levels of context conditioned fear responses and the interval of time between placement in the context and the occurrence of shock. These levels are directly related to that interval (Fanselow 1986;Kiernan and Westbrook 1993). Specifically, rats shocked a few minutes after placement in the context exhibit substantial levels of fear responses (e.g., freezing) because they had sufficient time before the shock to form the unitary representation required for context fear conditioning. Conversely, rats shocked at shorter placement-intervals freeze progressively less as the interval decreases. Indeed, rats shocked immediately on placement into the context exhibit little or no freezing-they exhibit the so-called immediate shock fear deficit (Fanselow 1980(Fanselow , 1986(Fanselow , 1990(Fanselow , 2010Kiernan and Westbrook 1993;Kierna...

Recent studies have shown that exposure to a novel environment may stabilize the persistence of weak memories, a phenomenon often attributed to a process referred to as "behavioral tagging." While this phenomenon has been repeatedly demonstrated in adult animals, no studies to date have examined whether it occurs in infant animals, which is surprising given that infants exhibit an impaired ability to form long-term memories (LTMs). In the present study, infant (i.e., postnatal day (P) 17) rats were placed in a context and repeatedly shocked. Infant rats given brief open field exposure 1 h, but not 2 h, prior to conditioning exhibited enhanced retention when tested 1 d later (Experiments 1 and 2), but comparable retention when tested shortly after training (Experiment 2). Thus, exploration of an open field facilitates subsequent context fear memories by enhancing the persistence of the memory rather than strengthening the context-shock association at encoding. While exploration of an open field did not lead to better memory when animals were tested 3 d later (Experiment 3), a brief pretest shock led to a more pronounced reinstatement effect in rats exposed to the open field 1 h before conditioning (Experiment 4). Finally, unlike what has been reported in adults, Experiments 5 and 6 suggest that familiarization of the open field before subsequent exposure does not abolish the behavioral tagging effect in infants. Overall, while these findings suggest that similar behavioral tagging mechanisms to those reported in adults might be involved in the formation of LTMs in infant rats, they also suggest that there may be developmental differences in the retention of familiarization experiences.

Behavioral tagging, which is well-established in adults, has recently been shown to also occur in infants. Interestingly, while familiarizing the novel experience abolishes behavioral tagging in adults, it appears to be without effect in infants. Familiarization, at least in infants, may act as an experience-dependent switch, closing the hippocampal critical period and thus accelerating the maturation of the hippocampus. In this study, infant (i.e., Postnatal Day 17) rats were placed in a context and shocked. Infants familiarized to an open field arena for 30 min the day before exhibited enhanced retention when tested 1 day later (Experiments 1and 2). While brief exploration of an open field soon before learning (i.e., the behavioral tagging procedure) resulted in better memory when rats were tested 1, but not 3, days later, familiarized rats had enhanced long-term memory (LTM) at both intervals (Experiment 3). Furthermore, familiarization, but not brief open field exposure, enhanced LTM for a nonhippocampal task (Experiment 4), suggesting that familiarization works through a different mechanism compared with behavioral tagging. Specifically, these results suggest that familiarization results in broader changes to the emotional learning and memory system rather than the hippocampus alone. Further investigation revealed that the effect of familiarization on LTM formation was mediated by isolation, rather than contextual novelty (Experiments 5 and 6), and consistent with this notion, maternal presence during familiarization blocked the enhancements in LTM (Experiment 7). Overall, these findings suggest that isolation during infancy may regulate the maturation of the emotional learning system.