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Reward behaviour is regulated by the strength of hippocampus–nucleus accumbens synapses

Author

Listed:
  • Tara A. LeGates

    (University of Maryland School of Medicine)

  • Mark D. Kvarta

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

  • Jessica R. Tooley

    (University of Maryland School of Medicine)

  • T. Chase Francis

    (University of Maryland School of Medicine)

  • Mary Kay Lobo

    (University of Maryland School of Medicine)

  • Meaghan C. Creed

    (University of Maryland School of Medicine)

  • Scott M. Thompson

    (University of Maryland School of Medicine
    University of Maryland School of Medicine)

Abstract

Reward drives motivated behaviours and is essential for survival, and therefore there is strong evolutionary pressure to retain contextual information about rewarding stimuli. This drive may be abnormally strong, such as in addiction, or weak, such as in depression, in which anhedonia (loss of pleasure in response to rewarding stimuli) is a prominent symptom. Hippocampal input to the shell of the nucleus accumbens (NAc) is important for driving NAc activity1,2 and activity-dependent modulation of the strength of this input may contribute to the proper regulation of goal-directed behaviours. However, there have been few robust descriptions of the mechanisms that underlie the induction or expression of long-term potentiation (LTP) at these synapses, and there is, to our knowledge, no evidence about whether such plasticity contributes to reward-related behaviour. Here we show that high-frequency activity induces LTP at hippocampus–NAc synapses in mice via canonical, but dopamine-independent, mechanisms. The induction of LTP at this synapse in vivo drives conditioned place preference, and activity at this synapse is required for conditioned place preference in response to a natural reward. Conversely, chronic stress, which induces anhedonia, decreases the strength of this synapse and impairs LTP, whereas antidepressant treatment is accompanied by a reversal of these stress-induced changes. We conclude that hippocampus–NAc synapses show activity-dependent plasticity and suggest that their strength may be critical for contextual reward behaviour.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:564:y:2018:i:7735:d:10.1038_s41586-018-0740-8
    DOI: 10.1038/s41586-018-0740-8
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    Citations

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    Cited by:

    1. Hiroyuki Kawai & Youcef Bouchekioua & Naoya Nishitani & Kazuhei Niitani & Shoma Izumi & Hinako Morishita & Chihiro Andoh & Yuma Nagai & Masashi Koda & Masako Hagiwara & Koji Toda & Hisashi Shirakawa &, 2022. "Median raphe serotonergic neurons projecting to the interpeduncular nucleus control preference and aversion," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    2. Candela Sánchez-Bellot & Rawan AlSubaie & Karyna Mishchanchuk & Ryan W. S. Wee & Andrew F. MacAskill, 2022. "Two opposing hippocampus to prefrontal cortex pathways for the control of approach and avoidance behaviour," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Joana Mendes Duarte & Robin Nguyen & Marios Kyprou & Kaizhen Li & Anastasija Milentijevic & Carlo Cerquetella & Thomas Forro & Stéphane Ciocchi, 2024. "Hippocampal contextualization of social rewards in mice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. 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.
    5. Irene Serra & Julio Esparza & Laura Delgado & Cristina Martín-Monteagudo & Margalida Puigròs & Petar Podlesniy & Ramón Trullás & Marta Navarrete, 2022. "Ca2+-modulated photoactivatable imaging reveals neuron-astrocyte glutamatergic circuitries within the nucleus accumbens," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Yun-Feng Zhang & Jialiang Wu & Yingqi Wang & Natalie L. Johnson & Janardhan P. Bhattarai & Guanqing Li & Wenqiang Wang & Camilo Guevara & Hannah Shoenhard & Marc V. Fuccillo & Daniel W. Wesson & Mingh, 2023. "Ventral striatal islands of Calleja neurons bidirectionally mediate depression-like behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Khairunisa Mohamad Ibrahim & Nicolas Massaly & Hye-Jean Yoon & Rossana Sandoval & Allie J. Widman & Robert J. Heuermann & Sidney Williams & William Post & Sulan Pathiranage & Tania Lintz & Azra Zec & , 2024. "Dorsal hippocampus to nucleus accumbens projections drive reinforcement via activation of accumbal dynorphin neurons," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Bahaaeddin Attaallah & Pierre Petitet & Rhea Zambellas & Sofia Toniolo & Maria Raquel Maio & Akke Ganse-Dumrath & Sarosh R. Irani & Sanjay G. Manohar & Masud Husain, 2024. "The role of the human hippocampus in decision-making under uncertainty," Nature Human Behaviour, Nature, vol. 8(7), pages 1366-1382, July.

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