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A hippocampus-accumbens code guides goal-directed appetitive behavior

Author

Listed:
  • Oliver Barnstedt

    (Leibniz Institute for Neurobiology
    German Center for Neurodegenerative Diseases (DZNE)
    Otto-von-Guericke University)

  • Petra Mocellin

    (Leibniz Institute for Neurobiology
    School for Brain & Behavior (IMPRS)
    University of California)

  • Stefan Remy

    (Leibniz Institute for Neurobiology
    German Center for Neurodegenerative Diseases (DZNE)
    Center for Behavioral Brain Sciences (CBBS)
    partner site Halle-Jena-Magdeburg)

Abstract

The dorsal hippocampus (dHPC) is a key brain region for the expression of spatial memories, such as navigating towards a learned reward location. The nucleus accumbens (NAc) is a prominent projection target of dHPC and implicated in value-based action selection. Yet, the contents of the dHPC→NAc information stream and their acute role in behavior remain largely unknown. Here, we found that optogenetic stimulation of the dHPC→NAc pathway while mice navigated towards a learned reward location was both necessary and sufficient for spatial memory-related appetitive behaviors. To understand the task-relevant coding properties of individual NAc-projecting hippocampal neurons (dHPC→NAc), we used in vivo dual-color two-photon imaging. In contrast to other dHPC neurons, the dHPC→NAc subpopulation contained more place cells, with enriched spatial tuning properties. This subpopulation also showed enhanced coding of non-spatial task-relevant behaviors such as deceleration and appetitive licking. A generalized linear model revealed enhanced conjunctive coding in dHPC→NAc neurons which improved the identification of the reward zone. We propose that dHPC routes specific reward-related spatial and behavioral state information to guide NAc action selection.

Suggested Citation

  • Oliver Barnstedt & Petra Mocellin & Stefan Remy, 2024. "A hippocampus-accumbens code guides goal-directed appetitive behavior," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47361-x
    DOI: 10.1038/s41467-024-47361-x
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    References listed on IDEAS

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    1. Christine Grienberger & Jeffrey C. Magee, 2022. "Entorhinal cortex directs learning-related changes in CA1 representations," Nature, Nature, vol. 611(7936), pages 554-562, November.
    2. Jason J. Moore & Jesse D. Cushman & Lavanya Acharya & Briana Popeney & Mayank R. Mehta, 2021. "Linking hippocampal multiplexed tuning, Hebbian plasticity and navigation," Nature, Nature, vol. 599(7885), pages 442-448, November.
    3. Johannes Felsenberg & Oliver Barnstedt & Paola Cognigni & Suewei Lin & Scott Waddell, 2017. "Re-evaluation of learned information in Drosophila," Nature, Nature, vol. 544(7649), pages 240-244, April.
    4. Kenneth D. Harris & Jozsef Csicsvari & Hajime Hirase & George Dragoi & György Buzsáki, 2003. "Organization of cell assemblies in the hippocampus," Nature, Nature, vol. 424(6948), pages 552-556, July.
    5. Garret D. Stuber & Dennis R. Sparta & Alice M. Stamatakis & Wieke A. van Leeuwen & Juanita E. Hardjoprajitno & Saemi Cho & Kay M. Tye & Kimberly A. Kempadoo & Feng Zhang & Karl Deisseroth & Antonello , 2011. "Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking," Nature, Nature, vol. 475(7356), pages 377-380, July.
    6. Seetha Krishnan & Chad Heer & Chery Cherian & Mark E. J. Sheffield, 2022. "Reward expectation extinction restructures and degrades CA1 spatial maps through loss of a dopaminergic reward proximity signal," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Christine Grienberger & Jeffrey C. Magee, 2022. "Author Correction: Entorhinal cortex directs learning-related changes in CA1 representations," Nature, Nature, vol. 612(7938), pages 8-8, December.
    8. Tara A. LeGates & Mark D. Kvarta & Jessica R. Tooley & T. Chase Francis & Mary Kay Lobo & Meaghan C. Creed & Scott M. Thompson, 2018. "Reward behaviour is regulated by the strength of hippocampus–nucleus accumbens synapses," Nature, Nature, vol. 564(7735), pages 258-262, December.
    9. Emilio Kropff & James E. Carmichael & May-Britt Moser & Edvard I. Moser, 2015. "Speed cells in the medial entorhinal cortex," Nature, Nature, vol. 523(7561), pages 419-424, July.
    10. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    11. Weilun Sun & Ilseob Choi & Stoyan Stoyanov & Oleg Senkov & Evgeni Ponimaskin & York Winter & Janelle M. P. Pakan & Alexander Dityatev, 2021. "Context value updating and multidimensional neuronal encoding in the retrosplenial cortex," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
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