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Coordinating brain-distributed network activities in memory resistant to extinction

Clarke-Williams, Charlie J; Lopes-dos-Santos, Vítor; Lefèvre, Laura; Brizee, Demi; Causse, Adrien A; Rothaermel, Roman; Hartwich, Katja; ... Dupret, David; + view all (2024) Coordinating brain-distributed network activities in memory resistant to extinction. Cell , 187 (2) 409-427.e19. 10.1016/j.cell.2023.12.018. Green open access

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Abstract

Certain memories resist extinction to continue invigorating maladaptive actions. The robustness of these memories could depend on their widely distributed implementation across populations of neurons in multiple brain regions. However, how dispersed neuronal activities are collectively organized to underpin a persistent memory-guided behavior remains unknown. To investigate this, we simultaneously monitored the prefrontal cortex, nucleus accumbens, amygdala, hippocampus, and ventral tegmental area (VTA) of the mouse brain from initial recall to post-extinction renewal of a memory involving cocaine experience. We uncover a higher-order pattern of short-lived beta-frequency (15–25 Hz) activities that are transiently coordinated across these networks during memory retrieval. The output of a divergent pathway from upstream VTA glutamatergic neurons, paced by a slower (4-Hz) oscillation, actuates this multi-network beta-band coactivation; its closed-loop phase-informed suppression prevents renewal of cocaine-biased behavior. Binding brain-distributed neural activities in this temporally structured manner may constitute an organizational principle of robust memory expression.

Type: Article
Title: Coordinating brain-distributed network activities in memory resistant to extinction
Open access status: An open access version is available from UCL Discovery
DOI: 10.1016/j.cell.2023.12.018
Publisher version: https://doi.org/10.1016/j.cell.2023.12.018
Language: English
Additional information: Copyright © 2023 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Keywords: Memory; hippocampus; prefrontal cortex; nucleus accumbens; amygdala; ventral tegmental area; oscillations; recall; renewal; extinction
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > UK Dementia Research Institute
URI: https://discovery.ucl.ac.uk/id/eprint/10204517
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