DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees

The activity of the epigenetic writers DNA methyltransferases (Dnmts) after olfactory reward conditioning is important for both stimulus-specific long-term memory (LTM) formation and extinction. It, however, remains unknown which components of memory formation Dnmts regulate (e.g. associative vs. no...

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Main Authors: Stephanie D Biergans, Judith Reinhard, Charles Claudianos, C Giovanni Galizia
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-09-01
Series:Frontiers in Molecular Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnmol.2016.00082/full
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spelling doaj-cf35800487da48429b9d85d36b27f2bf2020-11-24T23:02:31ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992016-09-01910.3389/fnmol.2016.00082215618DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybeesStephanie D Biergans0Stephanie D Biergans1Judith Reinhard2Charles Claudianos3Charles Claudianos4C Giovanni Galizia5University of QueenslandUniversität KonstanzUniversity of QueenslandUniversity of QueenslandMonash UniversityUniversität KonstanzThe activity of the epigenetic writers DNA methyltransferases (Dnmts) after olfactory reward conditioning is important for both stimulus-specific long-term memory (LTM) formation and extinction. It, however, remains unknown which components of memory formation Dnmts regulate (e.g. associative vs. non-associative) and in what context (e.g. varying training conditions). Here we address these aspects in order to clarify the role of Dnmt-mediated DNA methylation in memory formation. We used a pharmacological Dnmt inhibitor and classical appetitive conditioning in the honeybee Apis mellifera, a well characterized model for classical conditioning. We quantified the effect of DNA methylation on naïve odour and sugar responses, and on responses following olfactory reward conditioning. We show that (1) Dnmts do not influence naïve odour or sugar responses, (2) Dnmts do not affect the learning of new stimuli, but (3) Dnmts influence odour-coding, i.e. 'correct' (stimulus-specific) LTM formation. Particularly, Dnmts reduce memory specificity when experience is low (one-trial training), and increase memory specificity when experience is high (multiple-trial training), generating an ecologically more useful response to learning. (4) In reversal learning conditions, Dnmts are involved in regulating both excitatory (re-acquisition) and inhibitory (forgetting) processes.http://journal.frontiersin.org/Journal/10.3389/fnmol.2016.00082/fullDNA MethylationepigeneticsgeneralizationHoneybeememory formationmemory specificity
collection DOAJ
language English
format Article
sources DOAJ
author Stephanie D Biergans
Stephanie D Biergans
Judith Reinhard
Charles Claudianos
Charles Claudianos
C Giovanni Galizia
spellingShingle Stephanie D Biergans
Stephanie D Biergans
Judith Reinhard
Charles Claudianos
Charles Claudianos
C Giovanni Galizia
DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees
Frontiers in Molecular Neuroscience
DNA Methylation
epigenetics
generalization
Honeybee
memory formation
memory specificity
author_facet Stephanie D Biergans
Stephanie D Biergans
Judith Reinhard
Charles Claudianos
Charles Claudianos
C Giovanni Galizia
author_sort Stephanie D Biergans
title DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees
title_short DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees
title_full DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees
title_fullStr DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees
title_full_unstemmed DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees
title_sort dna methylation adjusts the specificity of memories depending on the learning context and promotes relearning in honeybees
publisher Frontiers Media S.A.
series Frontiers in Molecular Neuroscience
issn 1662-5099
publishDate 2016-09-01
description The activity of the epigenetic writers DNA methyltransferases (Dnmts) after olfactory reward conditioning is important for both stimulus-specific long-term memory (LTM) formation and extinction. It, however, remains unknown which components of memory formation Dnmts regulate (e.g. associative vs. non-associative) and in what context (e.g. varying training conditions). Here we address these aspects in order to clarify the role of Dnmt-mediated DNA methylation in memory formation. We used a pharmacological Dnmt inhibitor and classical appetitive conditioning in the honeybee Apis mellifera, a well characterized model for classical conditioning. We quantified the effect of DNA methylation on naïve odour and sugar responses, and on responses following olfactory reward conditioning. We show that (1) Dnmts do not influence naïve odour or sugar responses, (2) Dnmts do not affect the learning of new stimuli, but (3) Dnmts influence odour-coding, i.e. 'correct' (stimulus-specific) LTM formation. Particularly, Dnmts reduce memory specificity when experience is low (one-trial training), and increase memory specificity when experience is high (multiple-trial training), generating an ecologically more useful response to learning. (4) In reversal learning conditions, Dnmts are involved in regulating both excitatory (re-acquisition) and inhibitory (forgetting) processes.
topic DNA Methylation
epigenetics
generalization
Honeybee
memory formation
memory specificity
url http://journal.frontiersin.org/Journal/10.3389/fnmol.2016.00082/full
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