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Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction

Author

Listed:
  • Lars-Lennart Oettl

    (Heidelberg University
    Sainsbury Wellcome Centre for Neural Circuits and Behaviour)

  • Max Scheller

    (Heidelberg University)

  • Carla Filosa

    (Heidelberg University
    University Medical Center, Johannes Gutenberg University)

  • Sebastian Wieland

    (Heidelberg University)

  • Franziska Haag

    (Heidelberg University)

  • Cathrin Loeb

    (Heidelberg University)

  • Daniel Durstewitz

    (Heidelberg University)

  • Roman Shusterman

    (Institute of Neuroscience, University of Oregon)

  • Eleonora Russo

    (Heidelberg University)

  • Wolfgang Kelsch

    (Heidelberg University
    University Medical Center, Johannes Gutenberg University)

Abstract

The learning of stimulus-outcome associations allows for predictions about the environment. Ventral striatum and dopaminergic midbrain neurons form a larger network for generating reward prediction signals from sensory cues. Yet, the network plasticity mechanisms to generate predictive signals in these distributed circuits have not been entirely clarified. Also, direct evidence of the underlying interregional assembly formation and information transfer is still missing. Here we show that phasic dopamine is sufficient to reinforce the distinctness of stimulus representations in the ventral striatum even in the absence of reward. Upon such reinforcement, striatal stimulus encoding gives rise to interregional assemblies that drive dopaminergic neurons during stimulus-outcome learning. These assemblies dynamically encode the predicted reward value of conditioned stimuli. Together, our data reveal that ventral striatal and midbrain reward networks form a reinforcing loop to generate reward prediction coding.

Suggested Citation

  • Lars-Lennart Oettl & Max Scheller & Carla Filosa & Sebastian Wieland & Franziska Haag & Cathrin Loeb & Daniel Durstewitz & Roman Shusterman & Eleonora Russo & Wolfgang Kelsch, 2020. "Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17257-7
    DOI: 10.1038/s41467-020-17257-7
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    Cited by:

    1. David Wolf & Renée Hartig & Yi Zhuo & Max F. Scheller & Mirko Articus & Marcel Moor & Valery Grinevich & Christiane Linster & Eleonora Russo & Wolfgang Weber-Fahr & Jonathan R. Reinwald & Wolfgang Kel, 2024. "Oxytocin induces the formation of distinctive cortical representations and cognitions biased toward familiar mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Eleonora Russo & Nadine Becker & Aleks P. F. Domanski & Timothy Howe & Kipp Freud & Daniel Durstewitz & Matthew W. Jones, 2024. "Integration of rate and phase codes by hippocampal cell-assemblies supports flexible encoding of spatiotemporal context," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Laurens Winkelmeier & Carla Filosa & Renée Hartig & Max Scheller & Markus Sack & Jonathan R. Reinwald & Robert Becker & David Wolf & Martin Fungisai Gerchen & Alexander Sartorius & Andreas Meyer-Linde, 2022. "Striatal hub of dynamic and stabilized prediction coding in forebrain networks for olfactory reinforcement learning," Nature Communications, Nature, vol. 13(1), pages 1-21, December.

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