Human emotion and memory: interactions of the amygdala and hippocampal complex

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Abstract

The amygdala and hippocampal complex, two medial temporal lobe structures, are linked to two independent memory systems, each with unique characteristic functions. In emotional situations, these two systems interact in subtle but important ways. Specifically, the amygdala can modulate both the encoding and the storage of hippocampal-dependent memories. The hippocampal complex, by forming episodic representations of the emotional significance and interpretation of events, can influence the amygdala response when emotional stimuli are encountered. Although these are independent memory systems, they act in concert when emotion meets memory.

Introduction

One of the primary advances in the study of memory over the past half century is the growing recognition that there are multiple memory systems that are governed by distinct and interacting neural substrates [1]. Investigations examining the influence of emotion on memory have primarily focused on two medial temporal lobe memory systems (see Figure 1). The first is linked to the amygdala and is more or less specialized for the processing of emotion. The hallmark of this memory system is that it is crucial for the acquisition and expression of fear conditioning, in which a neutral stimulus acquires aversive properties by virtue of being paired with an aversive event. The second is linked to the hippocampal complex and is necessary for declarative or episodic memory. This memory system can be thought of as a primary memory system in humans, in that it governs the function most often referred to as ‘memory’, that is, the recollection of events at will.

Evidence that these two memory systems are independent comes from patients with focal lesions to the amygdala or hippocampus. In a classic fear conditioning paradigm, during which a neutral blue square is paired with an aversive shock to the wrist, patients with amygdala damage fail to show a normal physiological fear response to the blue square, even though they are able to report that the blue square predicted the shock [2]. Patients with damage to the hippocampus show the opposite pattern [3]. That is, they demonstrate a physiological arousal response to the blue square, but are not able to consciously recollect that it was paired with the shock. This double dissociation highlights the independent functions of these two memory systems. Even though these two systems can operate independently, they also interact in subtle and important ways. In this review, I outline how the amygdala and hippocampal complex influence each other when emotion and memory come together.

Section snippets

The amygdala’s role in hippocampal memory formation

Most research examining amygdala–hippocampal interactions has focused on how the amygdala can influence hippocampal-dependent, episodic memory for emotional stimuli. It is not surprising that there is abundant evidence that memories for emotional events have a persistence and vividness that other memories seem to lack [4]. The question is how does this occur? At least in part, the enhanced memory capability observed for emotional events is due to the amygdala’s influence on the encoding and

The influence of hippocampal-dependent memory on amygdala function

Although most of the research examining amygdala–hippocampal interactions has explored how the amygdala can influence episodic memory, there is also evidence of episodic memory influencing the amygdala. In the typical fear conditioning paradigm, a subject learns that a neutral stimulus predicts an aversive event by virtue of their pairing. In everyday human experience this type of learning often occurs. For example, if you were bitten by a neighborhood dog, the next time you encounter this dog

Conclusions

The amygdala and hippocampal complex govern two independent memory systems that interact when emotion meets memory. We are just beginning to understand the subtleties of these interactions in humans and there are still several unanswered questions.

Although we know more about the mechanisms that underlie the amygdala’s influence on hippocampal-dependent episodic memory, it is not clear how the modulation of attention and encoding complements the modulation of consolidation. It has been suggested

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

The author would like to acknowledge K Nearing and B Sedgewick for assistance with figure preparation and M Delgado for helpful comments.

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