The role of novelty and surprise in aversive conditioning

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Abstract Novelty and surprise have long been known to facilitate learning and memory. At a functional level this makes sense; unexpected events have to be learned about so they can be predicted and responded to appropriately in the future. At a psychological level, surprising events have been shown to enhance memory because they induce rehearsal. Subjects tend to “think about” unexpected events more than familiar ones after they occur. This has been observed directly in humans (explicit rehearsal) and indirectly in animals (implicit rehearsal). In both cases, the memory enhancement can be eliminated by disrupting rehearsal with a distractor stimulus that is presented immediately after the novel event. Presenting the same distractor stimulus several minutes later has no effect. This suggests rehearsal is short-lasting and distinct from the process of memory consolidation, which stabilizes new information for several hours after learning. In addition to increasing rehearsal, novel events also trigger the release of norepinephrine (NE) and dopamine (DA), which are known to enhance synaptic plasticity. Blocking receptors for these neuromodulators in the hippocampus prevents animals from forming new spatial and contextual memories. Based on these findings, we hypothesize that surprising events enhance memory because they induce catecholamine release at the same time the hippocampus is actively rehearsing/replaying new information. Our preliminary data demonstrate that NE and DA are both released in the hippocampus during and after the presentation of an unexpected aversive stimulus. At the same time, there is an increase in sharp-wave ripple oscillations (SWRs), which are known to contain replay sequences for recently encountered stimuli. Consequently, we will test the hypothesis above by monitoring and manipulating catecholamine release in real-time during an aversive learning task while simultaneously recording SWRs and imaging the activity of memory cells in the hippocampus.