Not "either-or" but "which-when": A review of the evidence for integration in sensory preconditioning.

• Sensory and emotional memories can be integrated in two ways. First, when the two memories share common content, the retrieval of one memory may call to mind the other, thereby allowing the sensory stimuli encoded as part of memory 1 to elicit responses that are appropriate to the emotional content of memory 2 ("memory chaining" at choice points). Second, as new emotional memories are encoded, past sensory memories can be activated and integrated with the emotional memory content ("online" integration), essentially resulting in formation of a false memory (or false memory content). • Here, we review studies of sensory preconditioning that have examined how sensory and emotional memories are integrated in the brain. We find that the two forms of integration are not mutually exclusive. That is, rather than the sensory and emotional memories that form in a preconditioning protocol being integrated in just one way or another, both forms of integration operate concurrently, with different protocols/parameters or training/test conditions increasing the likelihood of observing one form or another. • Chaining was observed in studies where the sensory stimuli presented in stage 1 of preconditioning were perceptually distinct, the emotional memory formed in stage 2 was very strong, and the context used for memory testing was highly familiar. • Online integration was observed in studies where the sensory stimuli presented in stage 1 of preconditioning were perceptually overlapping, the emotional memory formed in stage 2 was not over-trained, and the context used for memory testing was less familiar. Sensory preconditioning protocols can be used to assess how the brain integrates memories that share common features. In these protocols, animals are first exposed to pairings of two relatively innocuous stimuli, S2 and S1 (stage 1), and then to pairings of one of these stimuli, S1, with an event of motivational significance (stage 2). Following this training, test presentations of S2 elicit responses appropriate to the motivationally significant event, and these responses are taken to indicate formation of distinct S2-S1 and S1-event memories that are integrated in some way to generate that responding. This paper reviews studies of sensory preconditioning in rats, mice, rabbits and people to determine whether S2-S1 and S1-event memories are integrated through a chaining process at the time of their retrieval (i.e., test presentations of S2 trigger retrieval of S1, and thereby, responses appropriate to the event); or "online" at the time of memory formation (i.e., in stage 2, S1 activates a representation of S2 such that both stimuli associate with the motivationally significant event). It finds that the type of integration is determined by the manner in which stimuli are presented in preconditioning as well as their familiarity. When the stimuli in preconditioning are presented repeatedly and/or serially (i.e., one after the other), the S2-S1 and S1-event memories are chained at the time of retrieval/testing. In contrast, when the stimuli in preconditioning are relatively novel and/or presented simultaneously , the S2-S1 and S1-event memories are integrated online. These statements are related to prior claims regarding the circumstances that promote different types of memory integration and, more generally, mechanisms of information processing in the mammalian brain. [ABSTRACT FROM AUTHOR]