Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia

Long-term memory (LTM) is believed to be stored in the brain as changes in synaptic connections. Here, we show that LTM storage and synaptic change can be dissociated. Cocultures of Aplysia sensory and motor neurons were trained with spaced pulses of serotonin, which induces long-term facilitation....

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Main Authors: Shanping Chen, Diancai Cai, Kaycey Pearce, Philip Y-W Sun, Adam C Roberts, David L Glanzman
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2014-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/03896
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spelling doaj-a3e46fb1c8b9433498ce2c0372b1aa992021-05-04T23:31:38ZengeLife Sciences Publications LtdeLife2050-084X2014-11-01310.7554/eLife.03896Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in AplysiaShanping Chen0Diancai Cai1Kaycey Pearce2Philip Y-W Sun3Adam C Roberts4David L Glanzman5Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States; Department of Neurobiology, David Geffen School of Medicine at UCLA, Los Angeles, United States; Integrative Center for Learning and Memory, Brain Research Institute, University of California, Los Angeles, Los Angeles, United StatesLong-term memory (LTM) is believed to be stored in the brain as changes in synaptic connections. Here, we show that LTM storage and synaptic change can be dissociated. Cocultures of Aplysia sensory and motor neurons were trained with spaced pulses of serotonin, which induces long-term facilitation. Serotonin (5HT) triggered growth of new presynaptic varicosities, a synaptic mechanism of long-term sensitization. Following 5HT training, two antimnemonic treatments—reconsolidation blockade and inhibition of PKM—caused the number of presynaptic varicosities to revert to the original, pretraining value. Surprisingly, the final synaptic structure was not achieved by targeted retraction of the 5HT-induced varicosities but, rather, by an apparently arbitrary retraction of both 5HT-induced and original synapses. In addition, we find evidence that the LTM for sensitization persists covertly after its apparent elimination by the same antimnemonic treatments that erase learning-related synaptic growth. These results challenge the idea that stable synapses store long-term memories.https://elifesciences.org/articles/03896long-term memorysynaptic structurememory reconsolidationprotein kinase MζepigeneticAplysia californica
collection DOAJ
language English
format Article
sources DOAJ
author Shanping Chen
Diancai Cai
Kaycey Pearce
Philip Y-W Sun
Adam C Roberts
David L Glanzman
spellingShingle Shanping Chen
Diancai Cai
Kaycey Pearce
Philip Y-W Sun
Adam C Roberts
David L Glanzman
Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia
eLife
long-term memory
synaptic structure
memory reconsolidation
protein kinase Mζ
epigenetic
Aplysia californica
author_facet Shanping Chen
Diancai Cai
Kaycey Pearce
Philip Y-W Sun
Adam C Roberts
David L Glanzman
author_sort Shanping Chen
title Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia
title_short Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia
title_full Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia
title_fullStr Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia
title_full_unstemmed Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia
title_sort reinstatement of long-term memory following erasure of its behavioral and synaptic expression in aplysia
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2014-11-01
description Long-term memory (LTM) is believed to be stored in the brain as changes in synaptic connections. Here, we show that LTM storage and synaptic change can be dissociated. Cocultures of Aplysia sensory and motor neurons were trained with spaced pulses of serotonin, which induces long-term facilitation. Serotonin (5HT) triggered growth of new presynaptic varicosities, a synaptic mechanism of long-term sensitization. Following 5HT training, two antimnemonic treatments—reconsolidation blockade and inhibition of PKM—caused the number of presynaptic varicosities to revert to the original, pretraining value. Surprisingly, the final synaptic structure was not achieved by targeted retraction of the 5HT-induced varicosities but, rather, by an apparently arbitrary retraction of both 5HT-induced and original synapses. In addition, we find evidence that the LTM for sensitization persists covertly after its apparent elimination by the same antimnemonic treatments that erase learning-related synaptic growth. These results challenge the idea that stable synapses store long-term memories.
topic long-term memory
synaptic structure
memory reconsolidation
protein kinase Mζ
epigenetic
Aplysia californica
url https://elifesciences.org/articles/03896
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