Cited by 872Neural dynamics and brain functionMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

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Coherent Theta Oscillations and Reorganization of Spike Timing in the Hippocampal- Prefrontal Network upon Learning

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Benchenane, Karim, Peyrache, Adrien, Khamassi, Mehdi, Tierney, Patrick L., Gioanni, Yves, Battaglia, Francesco P., Wiener, Sidney I.·2010·Neuron

DOI 10.1016/j.neuron.2010.05.013

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Abstract

To study the interplay between hippocampus and medial prefrontal cortex (Pfc) and its importance for learning and memory consolidation, we measured the coherence in theta oscillations between these two structures in rats learning new rules on a Y maze. Coherence peaked at the choice point, most strongly after task rule acquisition. Simultaneously, Pfc pyramidal neurons reorganized their phase, concentrating at hippocampal theta trough, and synchronous cell assemblies emerged. This synchronous state may result from increased inhibition exerted by interneurons on pyramidal cells, as measured by cross-correlation, and could be modulated by dopamine: we found similar hippocampal-Pfc theta coherence increases and neuronal phase shifts following local administration of dopamine in Pfc of anesthetized rats. Pfc cell assemblies emerging during high coherence were preferentially replayed during subsequent sleep, concurrent with hippocampal sharp waves. Thus, hippocampal/prefrontal coherence could lead to synchronization of reward predicting activity in prefrontal networks, tagging it for subsequent memory consolidation.

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Authors: Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., & Wiener, S. I.
Affiliations: Centre National de la Recherche Scientifique (FR)
McGovern Institute for Brain Research (US)
Inserm (FR)
Corresponding author: Benchenane, Karim
Battaglia, Francesco P.
ORCID: Benchenane, Karim
Peyrache, Adrien
Khamassi, Mehdi
Battaglia, Francesco P.
Wiener, Sidney I.
Venue: Neuron
Publisher: Elsevier BV
Published: 2010-06
Volume: 66
Issue: 6
Pages: 921-936
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2010.05.013
OpenAlex: W2130674184
Cited by: 872
References: 73
Citations by year: 2026: 35 · 2025: 53 · 2024: 55 · 2023: 41 · 2022: 45 · 2021: 70 · 2020: 65 · 2019: 49 · 2018: 61 · 2017: 88 · 2016: 57 · 2015: 60 · 2014: 55 · 2013: 57 · 2012: 34
FWCI: 26.57
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1142 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
UvA-DARE (University of Amsterdam) (publishedVersion)
Radboud Repository (Radboud University) (submittedVersion)
HAL (submittedVersion, other-oa)
UvA-DARE (University of Amsterdam) (submittedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
Data Archiving and Networked Services (DANS) (submittedVersion)
Elsevier eBooks
Funders: Johns Hopkins University
Fondation Fyssen
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: hippocampus, medial prefrontal cortex, theta oscillations, neural coherence, spike timing, rule induction, Y-maze, memory consolidation, dopamine, interneurons, pyramidal neurons, sharp-wave ripples, reward prediction
MeSH terms: Action Potentials, Animals, Behavior, Animal, Dopamine, Hippocampus, Male, Neural Inhibition, Neural Pathways, Neurons, Periodicity, Reward, Spectrum Analysis, Time Factors, Prefrontal Cortex, Maze Learning, Rats, Long-Evans, Principal Component Analysis, Rats

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Coherent Theta Oscillations and Reorganization of Spike Timing in the Hippocampal- Prefrontal Network upon Learning

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