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The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats

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 underpinnin...

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Autores principales: Arkell, Daisy, Groves, Isabelle, Wood, Emma R., Hardt, Oliver
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8456983/
https://www.ncbi.nlm.nih.gov/pubmed/34526383
http://dx.doi.org/10.1101/lm.053256.120
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author Arkell, Daisy
Groves, Isabelle
Wood, Emma R.
Hardt, Oliver
author_facet Arkell, Daisy
Groves, Isabelle
Wood, Emma R.
Hardt, Oliver
author_sort Arkell, Daisy
collection PubMed
description 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.
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spelling pubmed-84569832021-10-01 The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats Arkell, Daisy Groves, Isabelle Wood, Emma R. Hardt, Oliver Learn Mem Research 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. Cold Spring Harbor Laboratory Press 2021-10 /pmc/articles/PMC8456983/ /pubmed/34526383 http://dx.doi.org/10.1101/lm.053256.120 Text en © 2021 Arkell et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by/4.0/This article, published in Learning & Memory, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Arkell, Daisy
Groves, Isabelle
Wood, Emma R.
Hardt, Oliver
The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats
title The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats
title_full The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats
title_fullStr The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats
title_full_unstemmed The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats
title_short The Black Box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats
title_sort black box effect: sensory stimulation after learning interferes with the retention of long-term object location memory in rats
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8456983/
https://www.ncbi.nlm.nih.gov/pubmed/34526383
http://dx.doi.org/10.1101/lm.053256.120
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