Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathways

IntroductionThe hippocampus and striatum have dissociable roles in memory and are necessary for spatial and procedural/cued learning, respectively. Emotionally charged, stressful events promote the use of striatal- over hippocampus-dependent learning through the activation of the amygdala. An emergi...

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Main Authors: Léa Tochon, Rose-Marie Vouimba, Marc Corio, Nadia Henkous, Daniel Béracochéa, Jean-Louis Guillou, Vincent David
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Psychiatry
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpsyt.2023.1129030/full
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author Léa Tochon
Rose-Marie Vouimba
Marc Corio
Nadia Henkous
Daniel Béracochéa
Jean-Louis Guillou
Vincent David
author_facet Léa Tochon
Rose-Marie Vouimba
Marc Corio
Nadia Henkous
Daniel Béracochéa
Jean-Louis Guillou
Vincent David
author_sort Léa Tochon
collection DOAJ
description IntroductionThe hippocampus and striatum have dissociable roles in memory and are necessary for spatial and procedural/cued learning, respectively. Emotionally charged, stressful events promote the use of striatal- over hippocampus-dependent learning through the activation of the amygdala. An emerging hypothesis suggests that chronic consumption of addictive drugs similarly disrupt spatial/declarative memory while facilitating striatum-dependent associative learning. This cognitive imbalance could contribute to maintain addictive behaviors and increase the risk of relapse.MethodsWe first examined, in C57BL/6 J male mice, whether chronic alcohol consumption (CAC) and alcohol withdrawal (AW) might modulate the respective use of spatial vs. single cue-based learning strategies, using a competition protocol in the Barnes maze task. We then performed in vivo electrophysiological studies in freely moving mice to assess learning-induced synaptic plasticity in both the basolateral amygdala (BLA) to dorsal hippocampus (dCA1) and BLA to dorsolateral striatum (DLS) pathways.ResultsWe found that both CAC and early AW promote the use of cue-dependent learning strategies, and potentiate plasticity in the BLA → DLS pathway while reducing the use of spatial memory and depressing BLA → dCA1 neurotransmission.DiscussionThese results support the view that CAC disrupt normal hippocampo-striatal interactions, and suggest that targeting this cognitive imbalance through spatial/declarative task training could be of great help to maintain protracted abstinence in alcoholic patients.
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spelling doaj.art-b87a3dc818a442af9d21aeda548e5d0f2023-05-26T04:19:49ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402023-05-011410.3389/fpsyt.2023.11290301129030Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathwaysLéa TochonRose-Marie VouimbaMarc CorioNadia HenkousDaniel BéracochéaJean-Louis GuillouVincent DavidIntroductionThe hippocampus and striatum have dissociable roles in memory and are necessary for spatial and procedural/cued learning, respectively. Emotionally charged, stressful events promote the use of striatal- over hippocampus-dependent learning through the activation of the amygdala. An emerging hypothesis suggests that chronic consumption of addictive drugs similarly disrupt spatial/declarative memory while facilitating striatum-dependent associative learning. This cognitive imbalance could contribute to maintain addictive behaviors and increase the risk of relapse.MethodsWe first examined, in C57BL/6 J male mice, whether chronic alcohol consumption (CAC) and alcohol withdrawal (AW) might modulate the respective use of spatial vs. single cue-based learning strategies, using a competition protocol in the Barnes maze task. We then performed in vivo electrophysiological studies in freely moving mice to assess learning-induced synaptic plasticity in both the basolateral amygdala (BLA) to dorsal hippocampus (dCA1) and BLA to dorsolateral striatum (DLS) pathways.ResultsWe found that both CAC and early AW promote the use of cue-dependent learning strategies, and potentiate plasticity in the BLA → DLS pathway while reducing the use of spatial memory and depressing BLA → dCA1 neurotransmission.DiscussionThese results support the view that CAC disrupt normal hippocampo-striatal interactions, and suggest that targeting this cognitive imbalance through spatial/declarative task training could be of great help to maintain protracted abstinence in alcoholic patients.https://www.frontiersin.org/articles/10.3389/fpsyt.2023.1129030/fullalcohollearning strategiesmemory systemshippocampus (CA1)dorsal striatumsynaptic plasticity
spellingShingle Léa Tochon
Rose-Marie Vouimba
Marc Corio
Nadia Henkous
Daniel Béracochéa
Jean-Louis Guillou
Vincent David
Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathways
Frontiers in Psychiatry
alcohol
learning strategies
memory systems
hippocampus (CA1)
dorsal striatum
synaptic plasticity
title Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathways
title_full Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathways
title_fullStr Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathways
title_full_unstemmed Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathways
title_short Chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum-dependent pathways
title_sort chronic alcohol consumption shifts learning strategies and synaptic plasticity from hippocampus to striatum dependent pathways
topic alcohol
learning strategies
memory systems
hippocampus (CA1)
dorsal striatum
synaptic plasticity
url https://www.frontiersin.org/articles/10.3389/fpsyt.2023.1129030/full
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