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Locus coeruleus and dopaminergic consolidation of everyday memory

Author

Listed:
  • Tomonori Takeuchi

    (Centre for Cognitive and Neural Systems, Edinburgh Neuroscience, The University of Edinburgh)

  • Adrian J. Duszkiewicz

    (Centre for Cognitive and Neural Systems, Edinburgh Neuroscience, The University of Edinburgh)

  • Alex Sonneborn

    (University of Texas Southwestern Medical Center)

  • Patrick A. Spooner

    (Centre for Cognitive and Neural Systems, Edinburgh Neuroscience, The University of Edinburgh)

  • Miwako Yamasaki

    (Hokkaido University Graduate School of Medicine)

  • Masahiko Watanabe

    (Hokkaido University Graduate School of Medicine)

  • Caroline C. Smith

    (University of Texas Southwestern Medical Center)

  • Guillén Fernández

    (Donders Institute for Brain, Cognition, and Behaviour, Radboud University Medical Centre)

  • Karl Deisseroth

    (Stanford University)

  • Robert W. Greene

    (University of Texas Southwestern Medical Center
    International Institute for Integrative Sleep Medicine (WPI-IIIS), University of Tsukuba)

  • Richard G. M. Morris

    (Centre for Cognitive and Neural Systems, Edinburgh Neuroscience, The University of Edinburgh
    Instituto de Neurociencias, CSIC-UMH)

Abstract

The retention of episodic-like memory is enhanced, in humans and animals, when something novel happens shortly before or after encoding. Using an everyday memory task in mice, we sought the neurons mediating this dopamine-dependent novelty effect, previously thought to originate exclusively from the tyrosine-hydroxylase-expressing (TH+) neurons in the ventral tegmental area. Here we report that neuronal firing in the locus coeruleus is especially sensitive to environmental novelty, locus coeruleus TH+ neurons project more profusely than ventral tegmental area TH+ neurons to the hippocampus, optogenetic activation of locus coeruleus TH+ neurons mimics the novelty effect, and this novelty-associated memory enhancement is unaffected by ventral tegmental area inactivation. Surprisingly, two effects of locus coeruleus TH+ photoactivation are sensitive to hippocampal D1/D5 receptor blockade and resistant to adrenoceptor blockade: memory enhancement and long-lasting potentiation of synaptic transmission in CA1 ex vivo. Thus, locus coeruleus TH+ neurons can mediate post-encoding memory enhancement in a manner consistent with possible co-release of dopamine in the hippocampus.

Suggested Citation

  • Tomonori Takeuchi & Adrian J. Duszkiewicz & Alex Sonneborn & Patrick A. Spooner & Miwako Yamasaki & Masahiko Watanabe & Caroline C. Smith & Guillén Fernández & Karl Deisseroth & Robert W. Greene & Ric, 2016. "Locus coeruleus and dopaminergic consolidation of everyday memory," Nature, Nature, vol. 537(7620), pages 357-362, September.
    • Handle: RePEc:nat:nature:v:537:y:2016:i:7620:d:10.1038_nature19325
    DOI: 10.1038/nature19325
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    Cited by:

    1. Fares J. P. Sayegh & Lionel Mouledous & Catherine Macri & Juliana Pi Macedo & Camille Lejards & Claire Rampon & Laure Verret & Lionel Dahan, 2024. "Ventral tegmental area dopamine projections to the hippocampus trigger long-term potentiation and contextual learning," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Yanjun Sun & Lisa M. Giocomo, 2022. "Neural circuit dynamics of drug-context associative learning in the mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Jia-Hou Poh & Mai-Anh T. Vu & Jessica K. Stanek & Abigail Hsiung & Tobias Egner & R. Alison Adcock, 2022. "Hippocampal convergence during anticipatory midbrain activation promotes subsequent memory formation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Florent Meyniel, 2020. "Brain dynamics for confidence-weighted learning," PLOS Computational Biology, Public Library of Science, vol. 16(6), pages 1-27, June.
    5. Xiaocen Fan & Jiachen Song & Chaonan Ma & Yanbo Lv & Feifei Wang & Lan Ma & Xing Liu, 2022. "Noradrenergic signaling mediates cortical early tagging and storage of remote memory," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Adrien T. Stanley & Michael R. Post & Clay Lacefield & David Sulzer & Maria Concetta Miniaci, 2023. "Norepinephrine release in the cerebellum contributes to aversive learning," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    7. Léonie Geissmann & David Coynel & Andreas Papassotiropoulos & Dominique J. F. Quervain, 2023. "Neurofunctional underpinnings of individual differences in visual episodic memory performance," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Nathan Bénac & G. Ezequiel Saraceno & Corey Butler & Nahoko Kuga & Yuya Nishimura & Taiki Yokoi & Ping Su & Takuya Sasaki & Mar Petit-Pedrol & Rémi Galland & Vincent Studer & Fang Liu & Yuji Ikegaya &, 2024. "Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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