Abstract

Author SummarySince Plato and the early cognitive psychologists we have believed that recollection is not a straightforward replay of stored experience; memory can be modified by the subject's experience and or state of mind, sometimes generating knowledge that was never itself experienced. We show in rats that direct neurophysiological evidence that episodic recollection is not a verbatim replay of stored experience; rather retrieval is a constructive process—an intermingling of the stored memory, environmental circumstances, and the subject's state of mind. To monitor internal, neural representations, we recorded the action potential discharge within a network of hippocampal neurons while rats performed two familiar active place avoidance tasks: one where the arena was stable and one where it rotated. Neural representations of the stable and rotating conditions were distinct. However, during the rotating task we intermittently observed intervals that we call “cross-episode retrieval” because discharge resembled the representation of the stable task. The incidence of cross-episode retrieval was higher when the angular position of the rotating arena was similar to that in the stable condition, demonstrating that retrieval is influenced by the environment. Cross-episode retrieval was also more likely when discharge represented the position of the rat in the stationary room rather than when it represented positions that rotate with the arena; this demonstrated that retrieval is influenced by internal cognitive variables that are encoded by hippocampal discharge—a state of mind. Thus novel, key features of constructive human episodic memory can be observed in rat hippocampal discharge.

Highlights

  • Cognitive psychologists have long understood that memory retrieval is not a straightforward reproduction of stored information but is rather aconstructive process that characteristically modifies the stored and recollected information [1]

  • We show in rats that direct neurophysiological evidence that episodic recollection is not a verbatim replay of stored experience; rather retrieval is a constructive process—an intermingling of the stored memory, environmental circumstances, and the subject’s state of mind

  • We examined ensemble discharge patterns of hippocampus CA1 principal neurons to evaluate three predictions of the constructive view: (1) discharge that is characteristic of the previously experienced condition and stored memory should co-express with the discharge that is characteristic of the current episode, demonstrating crossepisode retrieval; (2) external retrieval cues should influence the cross-episode expression of the memory-associated discharge; and (3) information in preretrieval hippocampal discharge should influence cross-episode retrieval of the memory-associated discharge

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Summary

Introduction

Cognitive psychologists have long understood that memory retrieval is not a straightforward reproduction of stored information but is rather a (re)constructive process that characteristically modifies the stored and recollected information [1]. The theory of constructive recollection asserts that information across different behavioral episodes may combine during recall to form what is recollected as a single experience. The theory of constructive recollection asserts that the retrieval cues can modify the content of the retrieved information. On the basis of such observations, the constructive theory has established that explicit memory retrieval is the result of complex interactions between the retrieval cues, information stored from prior experiences, and the subject’s state of mind. This process is known as ‘‘ecphoria’’ [5]

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