Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Emotional Learning Selectively Strengthens Memories


Nature  520, 345–348 (16 April 2015)

Emotional learning selectively and retroactively strengthens memories for related events

Joseph E. Dunsmoor,

Department of Psychology and Center for Neural Sciences, New York University, New York, New York 10003, USA

Nathan Kline Institute, Orangeburg, New York 10962, USA


Neurobiological models of long-term memory propose a mechanism by which initially weak memories are strengthened through subsequent activation that engages common neural pathways minutes to hours later. This synaptic tag-and-capture model has been hypothesized to explain how inconsequential information is selectively consolidated following salient experiences. Behavioural evidence for tag-and-capture is provided by rodent studies in which weak early memories are strengthened by future behavioural training. Whether a process of behavioural tagging occurs in humans to transform weak episodic memories into stable long-term memories is unknown. Here we show, in humans, that information is selectively consolidated if conceptually related information, putatively represented in a common neural substrate, is made salient through an emotional learning experience. Memory for neutral objects was selectively enhanced if other objects from the same category were paired with shock. Retroactive enhancements as a result of emotional learning were observed following a period of consolidation, but were not observed in an immediate memory test or for items strongly encoded before fear conditioning. These findings provide new evidence for a generalized retroactive memory enhancement, whereby inconsequential information can be retroactively credited as relevant, and therefore selectively remembered, if conceptually related information acquires salience in the future.

People are motivated to remember the episodic details of emotional events, because this information is useful for predicting and controlling important events in the future. In contrast, there is often little motivation to remember insignificant details we accumulate throughout the day, since much of this information is not associated with anything particularly meaningful. We do not always know, however, when a meaningful event will occur. From an adaptive memory perspective it is therefore critical that seemingly inconsequential details be stored in memory, at least temporarily, in the event that this information acquires relevance some time later. In this way, initially weak memories can be strengthened if this information later gains meaning. However, since we rarely encounter the same exact stimuli in the same exact situations it is advantageous for memories of other closely related information, encoded before a meaningful event, to be remembered as well. Such a mechanism could explain how a highly emotional event enhances memory for a host of details encoded earlier that, at the time, did not appear to hold any significance. Here, we provide evidence of a generalized retroactive memory enhancement in humans that is selective to information conceptually related to a future emotional event.

For episodic details to persist in long-term memory requires memory stabilization through the process of consolidation. A neurobiological account of memory consolidation has proposed a synaptic tag-and-capture mechanism whereby new memories that are initially weak and unstable are tagged for later stabilization by long-term potentiation (LTP) processes..This mechanism has been extended to the domain of hippocampus-dependent learning in rats to explain how weak behavioural training that would otherwise be forgotten will endure in memory following a new behavioural experience (for example, exposure to novelty)—an effect referred to as behavioural tagging.

Whether behavioural tagging occurs in human episodic memory is unknown. Evidence for such an effect would require that memory for older events that are related to subsequent experiences is selectively enhanced while other unrelated information encoded at the same time should not receive a retroactive memory benefit. While prior studies have shown post-encoding modulation of memory consolidation with increases in stress and arousal, these demonstrations do not provide evidence of specificity. Another strong test of this hypothesized process is to mitigate the potential for selective rehearsal by presenting information in the absence of any motivation or instruction to remember (incidental encoding) and conducting a surprise memory test. Finally, models of behavioural tagging predict memory strengthening for weak encoding, but not strong encoding. Thus, a task designed to retroactively boost relatively weak episodic memories should not retroactively benefit memories that were already strongly encoded.

Taking these criteria into consideration, we investigated whether information is selectively remembered if conceptually related information is later made salient through an amygdala-dependent learning task; that is, a trial-unique form of Pavlovian fear conditioning.

Our work provides new evidence for selective consolidation of information conceptually related to a future meaningful event. These findings support an implication proposed previously in the formulation of the synaptic tag-and-capture mechanism, that late-phase LTP of synaptic activity could explain enhanced memories for seemingly insignificant details surrounding emotional events. An intriguing implication of this finding concerns the adaptive nature of episodic memory. Specifically, humans and other animals continuously monitor the environment, accumulating countless details. Much of this information is forgotten. However, meaningful events can selectively preserve memory for previously encountered information that seemed insignificant at the time it was encoded. Whether such a mechanism contributes to persistent intrusive memories and overgeneralization of fear characteristic of trauma and stress-related disorders merits further empirical research.

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