Abstract

Reducing sensory experiences during the period that immediately follows learning improves long-term memory retention in healthy humans, and even preserves memory in patients with amnesia. To date, it is entirely unclear why this is the case, and identifying the neurobiological mechanisms underpinning this effect requires suitable animal models, which are currently lacking. Here, we describe a straightforward experimental procedure in rats that future studies can use to directly address this issue. Using this method, we replicated the central findings on quiet wakefulness obtained in humans: We show that rats that spent 1 h alone in a familiar dark and quiet chamber (the Black Box) after exploring two objects in an open field expressed long-term memory for the object locations 6 h later, while rats that instead directly went back into their home cage with their cage mates did not. We discovered that both visual stimulation and being together with conspecifics contributed to the memory loss in the home cage, as exposing rats either to light or to a cage mate in the Black Box was sufficient to disrupt memory for object locations. Our results suggest that in both rats and humans, everyday sensory experiences that normally follow learning in natural settings can interfere with processes that promote long-term memory retention, thereby causing forgetting in form of retroactive interference. The processes involved in this effect are not sleep-dependent because we prevented sleep in periods of reduced sensory experience. Our findings, which also have implications for research practices, describe a potentially useful method to study the neurobiological mechanisms that might explain why normal sensory processing after learning impairs memory both in healthy humans and in patients suffering from amnesia.

Highlights

  • In their original experiment, Jenkins and Dallenbach (1924) used sleep to reduce the amount of interference after learning

  • Sensory stimulation after learning impairs the retention of memory for object locations To test whether reducing sensory stimulation promotes memory retention in rats, we used a version of the spontaneous object exploration task that assesses long-term memory for object locations (Ennaceur and Delacour 1988)

  • Based on the findings with humans on the effects of quiet wakefulness on memory retention, we predicted that rats exposed to The Black Box after learning would retain memory for object locations better than rats that returned immediately to their home cage

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Summary

Introduction

In their original experiment, Jenkins and Dallenbach (1924) used sleep to reduce the amount of interference after learning. Jenkins and Dallenbach (1924) concluded that their results “indicate that forgetting is not so much a matter of the decay of old impressions and associations than a matter of the interference, inhibition, or obliteration of the old by the new.” Their findings were replicated by others, confirming that being asleep, compared with being awake and active, improves memory retention (Van Ormer 1932; Ekstrand 1967). Noting that participants in the sleep condition did not immediately fall asleep in the original experiment, but that they experienced increased quiescence shortly after learning, Minami and Dallenbach (1946) tested the retroactive interference explanation of forgetting more directly, by controlling the amount of stimulation after learning in awake animals. This lends strong support to the suggestion that the memory loss in amnesia arises from an increased vulnerability to interference shortly after encoding (Warrington and Weiskrantz 1974; Hardt et al 2013)

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